Review ArticleInsight on Rosaceae Family with Genome Sequencingand Functional Genomics Perspective
Prabhakaran Soundararajan So YounWon and Jung Sun Kim
Department of Agricultural Biotechnology National Institute of Agricultural Sciences RDA Jeonju 54874 Republic of Korea
Correspondence should be addressed to Jung Sun Kim jsnkimkoreakr
Received 21 September 2018 Revised 2 January 2019 Accepted 23 January 2019 Published 19 February 2019
Guest Editor Narendra Gupta
Copyright copy 2019 Prabhakaran Soundararajan et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited
Rosaceae is one of the important families possessing a variety of diversified plant species It includes many economically valuablecrops that provide nutritional and health benefits for the humanWhole genome sequences of valuable crop plants were released inrecent years Understanding of genomics helps to decipher the plant physiology and developmental process With the informationof cultivating species and its wild relative genomes genome sequence-basedmolecular markers andmapping loci for economicallyimportant traits can be used to accelerate the genome assisted breeding Identification and characterization of disease resistantcapacities and abiotic stress tolerance related genes are feasible to study across species with genome information Further breedingstudies based on the identification of gene loci for aesthetic values flowering molecular circuit controls fruit firmness nonacidfruits etc is required for producing new cultivars with valuable traits This review discusses the whole genome sequencing reportsofMalus Pyrus Fragaria Prunus and Rosa and status of functional genomics of representative traits in individual crops
1 Introduction
Rosaceae consists of 100 genera and 3000 species It is oneof the most economically important families which com-prised the fruit nut ornamental aroma herb and woodyplants Edible crops domesticated for human consumptionin Rosaceae include apple strawberry pear peach plumalmond raspberry sour cherry and sweet cherry Thoughmost of the choices are dietary based some of the vitalphytochemicals and antioxidants in fruits of Rosaceae havepotential to inhibit cancer For instance ellagic acid abundantin strawberry red raspberry and arctic bramble was shown toprevent cell proliferation and induce apoptosis of cancer cells[1 2]
Rosaceae consist of highly distinctive fruit types such asdrupe pome drupelet and achene Conventionally Rosaceaehas beendivided into four subfamilies based on the fruit typessuch as Rosoideae (several apocarpous pistils mature intoachenes) AmygdaloideaePrunoideae (single monocarpel-late pistil mature into a drupe) Spiraeaoideae (gynoeciumconsists of two or more apocarpous pistils mature intofollicles) andMaloideaePomoideae (ovary is compound and
inferior where floral receptacle is fleshy edible tissues) [3]Recently the phylogeny of Rosaceae has been divided intothree basal groups based on nuclear and chloroplast locinamely Amygdaloideae Rosoideae and Dryadoideae [1]Amygdaloideae has included the other subfamilies such asformer Amygdaloideae (n=8) (plum cherry apricot peachalmond etc) Spiraeaoideae (n=9) (Spiraea Aruncus Sor-baria etc) and Maloideae (n=17) (apple pear cotoneasteretc) Rosoideae (n=7) includes FragariaPotentilla Rosa andRubus Dryadoideae (n=9) includes Cercocarpus Chamaeba-tia Dryas and Purshia
Exhaustive breeding on fruit trees offered different typesof variety with variant alleles of genes controlling the keytraits To produce the sustainable cultivars we need toextend functional genomics studies in Rosaceae As Rosaceaeconsists of highly distinctive types of fruits and diversifiedgrowth patterns multiple genome models are required toimprove the agronomic practices produce high-yield anddisease resistance varieties overcome self-incompatibilityand reduce juvenile period long-lasting postharvest self-lifetolerant to chilling (storage) firmness against transportationdamage and higher nutritional content and health benefit
HindawiBioMed Research InternationalVolume 2019 Article ID 7519687 12 pageshttpsdoiorg10115520197519687
2 BioMed Research International
values An emergence of next-generation sequencing (NGS)technologies revolutionize biological field with its feasibilityto assemble and annotate any size and number of thegenome(s) [4] High-throughput genome sequencing offersthe substantial advantages for the explicit understandingof genetics and genomics [5] Recent breakthrough in thesequencing technologies and the availability of tools improvethe accuracy of de novo genome sequencing Unveiling thegenome information gives us an invaluable insight into theepigenetic characteristics [6] Genes responsible for traitsof agronomic importance are rapidly identified and char-acterized with the forward and reverse genetics studies onmany plants [4] Genome-wide association studies (GWAS)characterize the functional role(s) of gene [5] Genotyping-by-sequencing (GBS) and marker assisted selection (MAS)helps the precise breeding program [4] Genomics provideshuge amount of information in convenient manner for evo-lutional studies Comparative analysis among diverse plantfamilies helps to know about the evolutionary details of thegene(s)plant(s) [7] Candidate gene mapping in one speciesserves as a substrate for comparative analysis of other relatedspecies [5]
Therefore this review will cover the progress of NGS ofimportant commercial and model plants in Rosaceae suchas apple pear strawberry peach sweet cherry apricot androse Brief information about the functional genomics studiesconducted on critical key traits of the above-mentionedplants are also covered in this review
2 Genome Assembly and Annotation
Genome-scale study gives rich candidate genetic resourceto deciphering the functional and regulatory networks forgrowth and development NGS is the perfect platformto know about the genomic information which has wideapplication in crop improvement and evolutionary studiesGenome sequencing details of apple pear strawberry peachand rose have been given in Table 1 Desirable key traits willbe discussed in functional genomics section
21 Apple Apple fruit has higher nutritional values Forseveral centuries humans consumed apple-based beveragessuch as ciders [8] Malus x domestica or M pumila is thewidely growing apple tree Ancestor of domesticated Mdomestica is M sieversii It is originated in Central Asia(Southern China) Wild M pumila tree bearing smallersized fruits is still covered 80 of Tian Shan MountainsMicrosatellite markers study showed that M domestica isgenetically similar to European crabapple M sylvestris thanto the Asian wild appleM sieversii [9 10]
So far three genomes have been released in apple FirstlyVelasco et al (2010) covered 813 (6039Mb) of M xdomestica Borkh ldquoGolden Deliciousrdquo genome In that 57386geneswere identified Almost 674 ofM x domestica genomeconsists of repetitive sequences [11] Secondly Li et al (2016)covered about 90 (6324Mb) of M x domestica BorkhldquoGolden Deliciousrdquo genome A total number of identifiedprotein-coding and noncoding genes were 53922 and 2765respectively [12] Thirdly Daccord et al (2017) assembled
genome ofM x domestica Borkh ldquoGolden Delicious doubled-haploidrdquo line (GDDH13) Estimated genome size of GDDH13is 651Mb from which 6497Mb (998) was assembledHowever only 42140 protein-coding genes and 1965 non-protein coding genes were identified in GDDH13 genome[6] Major burst of transposable elements (TEs) happeningaround 21MYAwas correlatedwith the uplift of theTian Shanmountains as well as the diversification of apple and pear[11] Study on structural and functional evolution of genomecannot be completed without characterizing the TEs Around595 of the GDDH13 genome was covered with the TEelements Most interestingly HODOR (High-Copy GoldenDelicious repeat) TE consensus sequences are present atabout 223 Mb (36 of genome) [6]
22 Pear Pear is one of the most important temperate fruitIt is originated in Western China In spite of thousands ofcultivars based on the habituation Pyrus species are dividedinto two major groups such as Occidental pears or Europeanpears (P communis) and Oriental pears or Asiatic pears(P bretschneideri) [13] Nevertheless commercially importantcultivars were domesticated from the wide range of wildspecies still pear cultivation faces challenges such as suscepti-bility to the pear scab black spot disease self-incompatibilityearly ripening short shelf life firmness sucrose contentgritstone cells color and odor of fruit and inbreedingdepression [14]
Recently 971 of P bretschneideri Rehd (Chinese pear)genome ie 5120Mb (42812 genes) has been annotatedby Wu et al [15] Following it 5773Mb of P communis(European pear) was sequenced It covered around 984 ofgenome containing 43419 genes [16] Pear is phylogeneticallycloser towards the apple [1] Hence higher collinearity wasexisted between the chromosomes of pear and apple Pearand apple divergence could have happened only 54-215MYA [15] Presence of repetitive sequence about 531 in Pbretschneideri [15] and 345 in P communis [16] hamperedthe investigation of uncharacterized regions
23 Strawberry Strawberry comes under the category ofsoft fruit It is widely attracted for its aroma bright redcolor texture and taste Preservedprocessed strawberries arelargely used for ice creams milkshakes chocolates etc It isconsidered to be difficult to propagate
231 Fragaria vesca Fragaria vesca is a diploid speciesgenerally called woodland strawberry It has unique char-acteristics such as day neutrality nonrunning and yellowcolored fruits It is self-compatible and has short generationtime It is indigenous to northern Eurasia andNorth America[17]
Small genome (2400Mb) of strawberry (Fragaria vescaldquoHawaai4rdquo) showed the absence of whole genome duplica-tions Though all members of rosids shared the ancient tripli-cation no evidence of whole genome duplication was foundin F vesca About 998 (2395Mb) of genome was coveredwith identification of 33264 genes [17] Later Darwish et aldone the reference based reannotation and assembly of wood-land strawberry F vesca ldquoYW5AF7rdquo genome [18] Similar
BioMed Research International 3
Table1Genom
esequencingof
impo
rtantcom
mercialplantsbelong
stotheR
osaceaefam
ily
Com
mon
name
Samplen
ame
Chrn
umber
Genom
esize
Coverage()
Platform
Num
bero
fgenes
Repetitive
sequ
ences(Mb)
Reference
Estim
ated
(Mb)
Assembled
(Mb)
Apple
Mallusx
domesticaldquoG
oldenDelicou
srdquo
2n=2
x=34
7423
6039
813
BAC+454
57386
3623
Velascoetal2
010
Mallusx
domesticaldquo
GoldenDelicou
srdquo(H
eterologou
s)7010
6324
902
Illum
ina+
PacB
io53922
3820
Lietal2
016
Mallusx
domesticaldquoG
oldenDelicou
sdo
ubled-haploidrdquo
6510
6497
998
Illum
ina+
PacB
io4214
03722
Daccord
etal2
017
Pear
Pyrusb
retsc
hneid
erildquoDangshansulirdquo
2n=2
x=34
5120
5013
979
BAC-
by-BAC
+Illum
ina
42812
2402
Wuetal2
013
Pyruscom
mun
isldquoBartlettrdquo
6000
5773
962
454
43419
1977
Chagne
etal2
014
Strawberry
FragariavescasspvescaaccHaw
aii4
2n=2
x=14
2400
2395
998
Illum
ina+
454+
SOLiD
33264
498
Shulaeve
tal2010
Fragariaxananassa
ldquoReikourdquo
2n=8
x=56
6920
6977
1008lowast
454+Illum
ina
64947
3283
Hira
kawae
tal2014
Fragaria
iinum
ae
2n=2
x=14
2210
1996
903
26411
632
Fragarianipponica
2080
2065
993
21540
525
Fragarianu
bicola
2020
2037
1008lowast
21053
499
Fragariaorien
talis
3493
2142
613
17239
562
Chinesep
lum
and
Japanese
apric
otPrun
usmum
eldquoMeirdquo
2n=2
x=16
2800
237
846
Illum
ina
3139
01068
Zhangetal2
012
Peach
Prun
uspersica
ldquoLovellrdquov10
2n=2
x=16
2650
2246
847
BAC-
by-BAC
27852
8441
Verdee
tal2013
Prun
uspersica
ldquoLovellrdquov20
2274
858
Illum
ina
26873
-Ve
rdee
tal2017
Sweetcherry
Prun
usavium
ldquoSantonishikirdquo
2n=2
x=16
3800
2724
778
Illum
ina
43349
1194
Shira
sawae
tal2017
Rose
Rosa
chinensis
ldquoOld
Blushrdquo
2n=2
x=14
5600
5030
977
Illum
ina+
PacB
io3637
73415
Raym
ondetal2
018
Rosa
chinensis
ldquoOld
Blushrdquo
(dou
bled
haploid
ndashldquoHapOBrdquo)
5680plusmn
905120
901sim961
Illum
ina+
PacB
io44
481
2796
Saint-Oyant
etal
2018
Rosa
multifl
ora
750
711
948
Illum
ina
67380
4172
Nakam
urae
tal2018
lowastTh
ehighersizeo
fgenom
eassem
bled
than
thee
stimated
couldbe
either
duetolim
itatio
nin
thek
mer
abun
danceanalysisor
duplicationoccurringdu
ringtheg
enom
eassem
blyof
highlyrepetitiver
egion
4 BioMed Research International
to the macrosyntenic relationships between pear and appleFragaria shared the synteny with Prunus Lesser genome sizeof F vesca could be mainly due to the lack of highly abundantLTR retrotransposons (lt 2100 copies) Based on the obtainedgenome sequences 389 rosaceous conserved orthologous set(RosCOS) markers were developed in Rosaceae [19]
232 Fragaria x ananassa F x ananassa is commonlycultivated species that play an important role in the straw-berry production worldwide Interestingly F x ananassa wasreported as an accidental hybrid rose in France during mid-1700 between F chiloensis (Chile) and F virginiana (NorthAmerican cultivar) [17]
Genome size of this octoploid species F x ananassawas estimated between 708Mb and 720Mb F x ananassashared the genome information with wild diploids such asF iinumae F nipponica F nubicola and F orientalis andtheir genome size is 221Mb 208Mb 202Mb and 3493MbrespectivelyThe octaploid genome F x ananassawas assem-bled about 6977Mb and its wild relatives are as follows Fiinumae 1996 Mb (903) F nipponica 2064Mb (992) Fnubicola 2036Mb and F orientalis 2142 Mb (613) [20]In total the number of genes identified from F x ananassawas 230838 Protein-coding genes identified in wild relativesare 76760 in F iinumae 87803 in F nipponica 85062 inF nubicola and 99674 in F orientalis About 471 (3282Mb) of F x ananassa genome consists of repeats In case ofwild relatives 317 (633Mb) in F iinumae 255 (526Mb)in F nipponica 245 (499Mb) in F nubicola and 263(562Mb) in F orientalis are repeat regions in genome [20]
24 Prunus Prunus fruit has attractive bright shiny skincolor subtle flavor and sweetness It has long generation timeand bigger plant size It needs 3-5 years for floweringfruitproduction from planting Processed cherry product is soldworldwide
241 Chinese Plum and Japanese Apricot (Prunus mume)Prunus mume is the first plant in Prunoideae subfamilyto be sequenced Domestication of P mume could havestarted 3000 years ago in China [21] This woody perennialis considered as the first tree to be bloomed during thetransition from winter to spring at lesser than 0∘C [22]
Out of 280Mb of the genome size 2370Mb (846)was sequenced Totally 31390 protein-coding genes werecharacterized in the P mume Genome of P mume pro-vides information about the 1154 candidate genes involvedin flower aroma flowering time and disease resistanceAssembled genome contains 1068Mb (450) of repetitivesequences Investigation of P mume genome with the Vitisvinifera paleohexaploid ancestor showed that 27819 genemodels aligned with its seven ancestral chromosomes It isnoteworthy that 2772 orthologsrsquo (781) collinearity blockswere present in the P mume genome (Table 1) Comparativeanalysis of P mume chromosome with the Rosaceae ancestralchromosome showed that 4 5 and 7 chromosomes of Pmume does not undergo any changes and they are directRosaceae ancient chromosomes such as III VII and VIrespectively [23]
242 Peach (Prunus persica) Peach is one of great fruitthat provides vitamins minerals fiber and antioxidant com-pounds Peach fruit is also called nectarine due to smoothskin without fuzz or short hairs Selection and domesticationof peach could have started in Yangzi River valley Chinaaround 7500 years ago [24]
Whole genome analysis of P persica L ldquoLovellrdquo covered2246Mb (847) of genome (estimated total size 265Mb)and represented 27852 protein-coding genes Repetitivesequences present in peach were estimated as 8441Mb(3714) which is lesser than the apple (424) and grape(445) 6726Mb (2960) 2056 Mb (905) and 1714Mb(754) appeared as TEs DNA transposons and unclassifiedrepeats respectively [25] Recently P persica ldquoLovellrdquo doublehaploid genome version 20 was released with deep rese-quencing approach Assembled genome of 2274Mb (858)contains 26873 genes [26]
243 Sweet Cherry (Prunus avium) Prunus avium generallycalled sweet cherry is an important drupe fruit in the Rosaceafamily Sweet cherry is used for human consumption andwildcherry trees for wood which is also called mazzards Sweetcherry and sour cherry are the most commercial and ediblecrops in Prunus genus [27]
Genome size of P avium is about approximately 350MbShirasawa et al (2017) assembled about 778 (2724Mb) ofthe P avium ldquoSatonishikirdquo About 438 (1194Mb) of the Pavium genome were covered with the repetitive sequencesAmong the 1194Mb of repeats 851Mb of repeats are uniqueto P avium ldquoSatonishikirdquo Identified genes clustered with theP persica P mume M domestica and F vesca 75627 genesclusters are formed 3459 clusters (4535 genes) fromP aviumare present in all the investigated species and 16151 clusters(21642 genes) were found only in the P avium with theabsence of 869 clusters [28]
25 Rose Roses are one of the most essential ornamentalplants worldwide Ornamental value of rose enjoyed sincethe dawn of civilization Cultivation of roses traced back to3000 years ago It consists of 200 species and most of themare polyploid It has also been cultivated for its cosmeticvalues such as perfumes and antiques and also some of thephytochemicals of roses have high therapeutic values Rosehips can be used to cure osteoarthritis [29]
251 Rosa chinensis Rosa chinensis is one of the importantpot-type rose cultivars Recently Raymond et al (2018)sequenced the whole genome of R chinensis ldquoOld Blushrdquoand resequenced the major genotypes contributed for rosedomestication Totally 503Mb (977) of the genome wasassembled Genome results comprised 36377 protein-codinggenes 3971 long noncoding RNAs and 207 miRNAs In thegenome TEs were present about 679 From that 506were identified as long-terminal-repeat retrotransposons[30] From the doubled-haploid rose line of R chinensisldquoOld Blushrdquo (ldquoHapOBrdquo) about 901 to 961 (512Mb) ofgenomewas assembled About 466 Mbwas anchored to sevenpseudo-chromosomes and the remaining were assignedto the chromosome 0 (Chr0) Totally 44481 genes were
BioMed Research International 5
identified including 39669 protein-coding and 4812 noncod-ing genes Repeats covered about 2796Mb of genome [31]Rosa and Fragaria genomes shared the eight chromosomesof ancestral Rosaceae with one chromosome fission and twofusions Divergence of Rosa Fragaria and Rubus could haveoccurred within a short period [30] Synteny analysis showedthat chromosomes 1 4 5 6 and 7 of R chinensis havehigher collinearity with chromosomes 7 4 3 2 and 5 of Fvesca Interestingly chromosomes 2 and 3 of R chinensisweredetected as reciprocal translocation with chromosomes 6 and1 of F vesca [31]
252 Rosa multiflora Rosa multiflora is a five-petal plantbelongs to the section Synstylae It is native to the easternAsian regions [32] R multiflora was used for breedingpurpose to the modern roses Especially its resistance locus(Rdr1) tolerance against powdery mildew was introgressedwith the R hybrida [33]
Genome size of R multiflora was estimated as 750Mband about 711Mb was sequenced Assembled genome wascharacterized with 67380 genes (54893 complete genesand 12487 partial genes) Repeat regions covered 564(4172Mb) of assembled genome Out of 18956 gene clustersin R multiflora 1287 904 and 241 clusters were shared withthe F vesca P persica and M x domestica respectively Rmultiflora shared more number of gene clusters with theF vesca than the other two plants of Rosaceae Howeverunique gene clusters and genes of R multiflora are 25 (3482of R multiflora and 1397 of F vesca) and 33 (14663 of Rmultiflora and 4482 of F vesca) times higher than the F vescarespectively [34]
3 Functional Genomics
31 Fruit Development and Sucrose Metabolism in ApplePome is a unique nature of false fruit formation from thebasal part of sepals and receptacles Velasco et al (2010)suggest that pome could have evolved recently from Maleaespecific WGD which could be a major factor contributing toapple development and its specificity [11] Genes encodingfor like-hetero chromatin protein 1 (LHP1) such asMdLHP1aand MdLHP1b regulate the flowering time of apple [35]Flowering locus T1 (MdFT1) can promote flowering whereasterminal flower (MdTFL1 and MdTFL2) expressed in thevegetative part could repress flowering and maintains thevegetative meristem identity [36] Soon after fertilizationhigher expression of two cyclin-dependent kinase (CDK)bgenes and one cyclin-dependent kinase regulatory subunit(CKS) 1 indicates the active cell division of fruits [37] Tran-scription factors such asAgamous (AG) Fruitfull (FUL) AG-like (AGL)1AGL5 Spatula (SPT) Crabs Claw (CRC) andEttin (ETT) regulate the carpel identity and differentiation[38] Microarray data on apple reported that SPT ETTAuxinResponse Factor (ARF) 3 FULAGL8 and CRC transcriptswere abundant during the fruit enlargement stage Howevermost of their expressions are downregulated in cell divisionstage [39] In apple fruit development-related gene familiessuch asMADS-box genes carbohydrate metabolism sorbitolassimilation and transportation were expanded more than
the cucumber soybean poplar A thaliana grape riceBrachypodium sorghum and maize [11] Expression of 120572-expansin (120572-EXP)was detected only during the cell expansionphase of apple [39] MdMADS21 and MdMADS22 orthol-ogous to FUL-like genes in A thaliana were progressivelyinvolved in the fruit developmental process Among twocandidate genes MdMADS21 was closely associated withfruit flesh firmness [40] ARF106 gene expressed duringcell division and cell expansion stages is consistent with apotential role in the control of fruit size [41] Methylation ofDNAplays an essential role in the fruit size [12] Comparativestudy between the bigger size apple (Golden Delicious) andsmaller size apple (GDDH18) showed that twenty-two genesfound as responsible for small size have lesser methylation inthe promoter region [6]
After pollination the small amount of starch present inthe floral buds starts to metabolize Conversion of carbonto sucrose was mediated by the tonoplast monosaccharidetransporters (TMTs) MdTMT1 and MdTMT2 Expansion offruit cells is associated with the starch accumulation Higherexpression of sorbitol dehydrogenase (SHD) cell wall invertase(CIN) neutral invertase (NIN) sucrose synthase (SS) fruc-tokinase (FRK) and hexokinase (HK) indicates the metabo-lization of sorbitol and sucrose [42] In the early period ofcell expansion starch accumulation was higher and it startsto decline in the later phase [11] Transcript of SS genes inapple is correlated with the starch accumulation [39] Sorbitoldehydrogenase (SDH) converts carbohydrate into fructoseNine SDH genes were identified in apple fruit [43] In youngfruit MdSDH1 expression was higher than in mature fruit[42] Other genes significantly upregulated during ripeningstage are isopentenyl pyrophosphate (IPP) isomerase catalase(CAT) histone 2B (H2B) and the ripening-inhibitor (RIN)MADS-box gene [39] During the ripening process a decreaseof starch synthesis is vice versa with the sugar level [44]Expression profiles of sucrose-phosphatase phosphatase (SPP)and sucrose-phosphate synthase (SPS) were active in the ripen-ing stage [42] suggesting that these enzymesmay be involvedin starch degradation pathway Polygalacturonase 1 (MdPG1)and aminocyclopropane-1-carboxylate oxidase (MdACO1)were involved in the fruit softening and ethylene biosynthesisin apple respectively [45] Decrease in the expression ofPG1 alters the firmness tensile strength and water loss inapple M x domestica fruit [46] MeanwhileMdFT1MdACS1(1-aminocyclopropane-1-carboxylic acid synthase) MdACO1and MdExp7 are regulating the fruit softening Amongthem MdExp7 and MdACO1 control firmness in apple [45]Gene coding for MYB TF in apple MdMyb1 increases theanthocyanin content and is responsible for the red skin color[47] Acidity in apple is due to the malic acid and mamarecessive gene is responsible for low acidity [48]
In apple fruit size sugar content and palatability areessential qualities determining its marketability Knowledgeof genes governing the fruit quality could be essential forscreening better linesgenotypes for breeding
32 Lignin Metabolism and Stone Cell Formation in PearStone cell content is the main quality determinant of pearfruit Deposition of lignin on the primary cell wall of
6 BioMed Research International
Lignin synthesis
Branchy sclereids
Stone cells
HCT
LIMMYB
PbCAD2
PbCCR2
PbCCR1
PbCCR3
CCOMTC3H
NAC (NAM ATAF12 and CUC2)
Figure 1 Simple heuristic representation of genestranscription factors involved in lignin synthesis and stone cell formation in pearfruit Pb Pyrus bretschneideri hydroxycinnamoyl transferase HCT p-coumaroyl-shikimatequinate 31015840-hydroxylases C31015840H caffeoyl-CoA O-methyltransferase CCOMT NAM ATAF12 and CUC2 NAC Lin11Isl1Mec3 LIM myeloblastosis MYB cinnamyl alcohol dehydrogenaseCAD and cinnamoyl-CoA reductase CCR Red colored dots represent the stone cells
parenchyma cell followed by the secondary sedimentation ona sclerenchyma cell forms the stone cells Majority of stonecells present in pear is branchy sclereids comprised lignin andcellulose Lignins are synthesized by twoways one starts withp-coumaric acid and second with phenylalanine precursorto cinnamic acid and then p-coumaric acid Other forms oflignin monomers are caffeic acid ferulic acid 5-hydroxy-ferulic acid and sinapinic acid [49ndash51] Finallymonomers arepolymerized to form lignin products Monomers of lignin arecategorized into three types syringly lignin (S-lignin) guaia-cyl lignin (G-lignin) and hydroxyphenyl lignin (H-lignin)From the gnome analysis a total of 66 lignin synthesis-related gene families were characterized in P bretschneideriIt signifies the high demand for lignin synthesis in pear [15]In ldquoDangshan Surdquo pulp milled wood lignin was identifiedas guaiacyl-syringyl-lignin It was observed that ldquoDangshanSurdquo lignin possesses more guaiacyl units than the syringylunits [49] Hydroxycinnamoyl transferases (HCT) play asignificant role in the lignin synthesis [52] Accumulation ofG-lignin and S-lignin is interrelated with theHCT expressionespecially at early fruit developmental stage [15]
Cinnamoyl-CoA reductase (CCR) and cinnamyl alco-hol dehydrogenase (CAD) belonging to medium-or-short-chain dehydrogenasereductase are key enzymes for ligninmonomer synthesis [53] Totally 31 CCRs and 26 CADsgenes were identified in P bretschneideri ldquoDangshan Surdquo Allmembers of CCR and CAD identified in P bretschneideri arenot involved in the lignin biosynthesis [54] Among them
PbCAD2 PbCCR1 PbCCR2 and PbCCR3 were identified toparticipate in the lignin synthesis of stone cells [15] NAC(NAM ATAF12 and CUC2) and LIM (Lin11Isl1Mec3) arean important TF influencing the lignin pathway [55 56]Mostof theCCR andCADmembers present in the pear possess SPL(squamosal promoter binding-like) light-responsive elementon their upstream Functions of PbCCR and PbCAD arerelated to the light signaling Presence of MYB-binding ACcis elements in some promoter of the PbCCRs suggestedthat phenylpropanoid metabolism of lignin synthesis wasregulated by MYB transcription factors Similarly TGACG-motif on some PbCCRs and all PbCADrsquos promoter regionsrevealed their involvement in the abscisic acid jasmonicacid andmethyl jasmonic acidmetabolism [15]The pictorialillustration of genesTFs required for the lignin synthesis aswell as stone cell formation is mentioned in Figure 1
There are many internal and external factors involved inthe stone cell formation of pear Identification of candidategenes of lignin biosynthesis and stone cell formation willbe very much useful to improve the cultural practices forproducing pear fruits with different palatable level of stonecells
33 Fruit Aroma and Softness in Strawberry Strawberry iswidely appreciated for its delicate flavor aroma and nutri-tional value Aroma of strawberry is due to esters alcoholsaldehydes and sulfur compounds Hundreds of volatile estershave been correlated with strawberry ripening and aroma
BioMed Research International 7
[57] Volatile esters are the major constituents of floral scentWild species such as F vesca and F virginiana have muchstronger aroma than the cultivated types Compared to theregular octoploid strawberry unique phenolic compoundswere found inF vesca fruits such as taxifolin 3-O-arabinosideand peonidin 3-O-malonylglucoside [58] Pinene synthase(PINS) is primarily expressed in wild strawberry whileinsertional mutation reduced its expression in cultivatedspecies F vesca contains high amounts of ethyl-acetate andlower methyl-butyrate ethyl-butyrate and furanone levels Fnilgerrensis possesses higher ethyl-acetate and furanone butlower methyl-butyrate and ethyl-butyrate Hybrids betweenF vesca and F ananassa have intermediate contents of fra-grance and aroma related compounds while crosses betweenF nilgerrensis and F ananassa more closely resemble Fnilgerrensis [17] Volatile compounds found to be responsiblefor general strawberry smell are 2 5-dimethyl-4-hydroxy-3(2H)-furanone linalool and ethyl hexanoate Neverthelessethyl butanoate methyl butanoate 120574-decalactone and 2-heptanone are represented as cultivar specific aroma com-pounds [59] O-methyltransferase of strawberry (FaOMT) isvital for the biosynthesis of vanillin and furaneol [60]Alcoholacyltransferase (AATs) in strawberry (SAAT) is involved inthe last step of volatile esters synthesis and vital for flavorbiogenesis in ripening fruit SAAT catalyzes esterificationof an acyl moiety from actyl-CoA to alcohol [61] Straw-berry quinone oxidoreductase (FaQR) is required for thebiosynthesis of furaneol Furaneol and its methoxy derivative(methoxyfuraneol and mesifuran) are catalyzed by OMT Allthree furaneol compounds are highly accumulated duringfruit ripening stage [62] Though two types of pyruvatedecarboxylase (PDC) were identified in strawberry onlyFaPDC1 was induced during fruit ripening [63]
Strawberry is highly perishable even with controlledatmospheric storage Higher proportion of fruit last occurreddue to its softness and sensitivity to fungal disease Redcolored strawberry showed the higher level of anthocyanin-related transcripts [64] FcMYB1 could regulate branching-point of the anthocyaninproanthocyanidin biosynthesisFaWRKY1 mediate defense response and FaPE1 encodedfor pectin methyl esterase are conferred at least with apartial resistance of ripened fruit against Botrytis cinerea[65 66] Polygalacturonase 1 of F x ananassa (FaPG1) iscritical for fruit softening [67] In strawberry fruits beta-D-glucosyltransferase (FaGT) correlated with the relevantphenylpropanoid glucosides [68]D-xylose reductase (FaXyl1)and beta-xylosidase activity were higher in ldquoToyonakardquo (soft)than in the ldquoCamarosardquo (firm) showing the correlationbetween FaXyl1 expression and fruit softening [69] Fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase) is involvedin the firmness and postharvest life [70] A lesser activity ofbeta-galactosidase (120573Gal) and 120573Xyl activity were correlatedwith decreased fruit firmness in F chiloensis and F timesananassa respectively [71] Expression of FaCCR is higherin soft fruit cultivar (Gorella) whereas FaCAD is higher infirm fruit cultivar (Holiday) [72] Expression of five expansingenes (FaEXP1 FaEXP2 FaEXP4 FaEXP5 and FaEXP6) wasstudied in cultivars with different firmness ldquoSelvardquo (hard)ldquoCamarosardquo (medium) and ldquoToyonakardquo (soft) Higher level
of FaEXP1 FaEXP2 and FaEXP5 expression was foundin fruit with less firmness (ldquoToyonakardquo) than the othertwo cultivars (ldquoSelvardquo and ldquoCamarosardquo) Fruit firmnessis identified to be associated with pectate lyase (FaPel1)identified Expansin activity was characterized by cell wallmodification [73] Polysaccharides were modified by fivedifferent genes such as FasPG FaPG-like FaPel1 FaPel2 andFaEXP2 [74] Sorbitol dehydrogenase (FaSDH) and sorbitol-6-phosphate dehydrogenase (FaS6PDH) genes are involved withthe sorbitol synthesis in leaves fruits and shoot tips [75]SEPALLATA (SEP)4-like gene FaMADS9 is responsible forthe fruit ripening [76]
Apart from the aesthetic and taste mechanisms of flower-ing and its response to the light signaling in strawberry needto be studied in detail Cultivars with continuous floweringand growing underminimal light energy are beneficial for thestrawberry growers as most of the commercial cultivation iscarried out in the controlled greenhouse
34 Early Blooming and Fruit Ripening in Prunus Prunusis the first plant to bloom in later winterearly spring Soit is the best model plant to study early flowering as wellas chilling tolerance Dehydrins are known as 2 or D-11family late-embryogenesis-abundant (LEA) proteins Theyplay a vital role in plant growth and cold tolerance [77] InP mume 30 LEA genes were characterized and classifiedinto eight groups LEA1 LEA2 LEA3 LEA4 LEA5 PvLEA18dehydrin and seed maturation protein Out of 30 identifiedgenes 22 were expressed in flowers and 19 were inducedby abscisic acid (ABA) treatments [78] Molecular cloningof PmLEA8 PmLEA10 PmLEA19 PmLEA20 and PmLEA29showed that except PmLEA8 all other genes enhancedthe freezing-tolerance Interestingly among all cold-resistantLEA genemembers studied only PmLEA19were upregulatedfour timeswhen the branches of Pmumewere exposed to 4∘C[79]Downregulation inPmume dormancy associatedMADS(PmDAM) 4 PmDAM5 and PmDAM6 expression releasesthe endodormancy [80] Among the six DAM genes exceptPmDAM3 all other genes are responsive to the photoperiodand seasonal (cold) responses [81] In P persica from six iden-tified DAM genes PpDAM5 and PpDAM6 were character-ized to be involved in the lateral bud dormancy breakage [82]DAM5 and DAM6 were identified as homologous to ShortVegetative Phase (SVP)AGL 24 in A thaliana Both SVPand AGL-24 are required for floral meristem identity [83]AGL24 is well known for promoting early flowering and floraltransition in plants [58] Transcriptome analysis betweencold sensitive (ldquoMorettinirdquo) and cold tolerant (ldquoRoyal Gloryrdquo)cultivars in P persica showed that 120573-D-xylosidase (BXL)and pathogen-related protein 4b (PR-4B) were significantlyexpressed only in resistant variety [84] Other candidategenes identified as required to control flowering time aresuppressor of phyA (SPA) COP1 interacting protein8 (CIP8)phytochrome A (phyA) and phytochrome interacting factor 3(PIF3) [85] Figure 2 demonstrates the important key genesinvolved in cold tolerance early blooming and floweringtime control of P mume Higher number of aesthetic prop-erties related genes such as benzyl alcohol acetyltransferase(BEAT) (34) are identified in P mume Only 16 in Malus x
8 BioMed Research International
PmLEA19 PmDAM4 PmDAM5 and PmDAM6
SPA CIP8 phyA and PIF3BXL and PR-4B
Cold toler
ance
Cold tolerance
Control flowering time
Dorman
cy re
lease
Figure 2 Factors involved in the early blooming of Chinese plumJapanese apricot Prunus meme Pm late-embryogenesis-abundant LEAdormancy associated MADS DAM 120573-D-xylosidase BXL pathogen-related protein 4b PR-4B suppressor of phyA SPA COP1 interactingprotein8 CIP8 phytochrome A phyA and phytochrome interacting factor3 PIF3 The lower arrow represents downregulation
domestica 14 in F vesca 4 inVitis vinifera 17 in P trichocarpaand 3 inA thaliana of BEAT genes were identifiedThereforein P mume BEAT genes are considered as key factor todetermine its exclusive floral fragrance [23]
In Prunus UDP-glucose-flavonoid-3-O-glucosyltransfer-ase (UFGT) expression was higher during the initial periodand it is reduced on the developmental process Duringthe ripening processMYB10 MYB123 and basic-helix-loop-helix (bHLH3)were upregulatedwhereasMYB16 andMYB111were downregulated Higher anthocyanin and Proantho-cyanidin levels were correlatedwith theMYB10 andMYBPA1respectively Stimulation of TFs is responsive for the devel-opment and external stimuli [86] Gene encoding ethylene-responsive transcription factor (ERF)4 is necessary for the fruitmaturity [87] Though 74 EFR genes were predicted in thepeach genome only one copy of ERF4 has existed ThereforeERF4 is vital to control the fruit maturity and ripening inpeach [85] An initial stage of fruit has higher aldehyde andalcohol production whereas later stages have lesser contentwhich is correlated with the ester production Abundance ofalcohol dehydrogenase (ADH) and lipoxygenase (LOX) geneis constant in the fruit development stages Expression ofAATwas sharply increased in the later stage of harvest [88] Rapidsoftening of fruits was related to the ethylene productionin P persica It is correlated with expression of PpACS1 (1-aminocyclopropane-1-carboxylic acid synthase) [89] Ripenedsweet cherry P avium has unique fragrance In the sweetcherry (ldquoHongdengrdquo ldquoHongyanrdquo and ldquoRainierrdquo) 97 volatilecompounds were identified Alcohols and terpenes were thepredominant components of bound volatiles Benzyl alcoholgeraniol and 2-phenylethanol are the major bound volatileconstituents Free volatile compounds majorly present insweet cherry are hexanal 2-hexenal 2-hexen-1-ol benzyl
alcohol and benzaldehyde Free volatiles are responsible forfloral aroma and bound volatiles involved in fruit freshnessDepending on the level of free and bound volatiles aroma andglycosidically bound compounds aroma and fruit firmnesswere varied between the cultivars of sweet cherry [90]
In Prunus apricot peach sweet cherry and sour cherryare widely used for human consumption Comparativegenomics study between the species offer the candidate geneto produce hybrids with more preferable qualities
35 Blooming and Scent Pathways in Rose Continuous flow-ering (CF)recurrent blooming (RB) genotypes flowers in allfavorable seasons whereas once-flowering (OF) genotypesonly flowers in spring Recurrent blooming is an importanttrait required by breeders R x hybrida ldquoLa Francerdquo was thefirst hybrid combined with the growth vigor of Europeanspecies and recurrent blooming of Chinese species It hasthe complex genetic pool combination of three ancestralgenotypes such as Cinnamomeae Synstylae and ChinensesInsertion of TE in the TFL1 encodes gene Ksncopia (KSN)was found as responsible for the recurrent blooming of ldquoLaFrancerdquo [30] Previously Horibe et al (2013) reported thatKSN gene regulates the CF behavior of R rugosa [91] Wanget al (2012) studied recurrent flowering character and theexpression patterns of TFL1 homologs in R multiflora Rrugosa R chinensis and other speciescultivars Among thethree orthologs RTFL1c was highly expressed at all fourflowering stages in R multiflora and R rugosa (nonrecurrentflowering species) and barely detected in R chinensis (arecurrent flowering species) at any stage Therefore it can beconsidered that lower expression of RTFL1c is required forrecurrent flowering of roses [92] Iwata et al (2012) elucidatethat occurrence of TE insertion and point mutation in the
BioMed Research International 9
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
values An emergence of next-generation sequencing (NGS)technologies revolutionize biological field with its feasibilityto assemble and annotate any size and number of thegenome(s) [4] High-throughput genome sequencing offersthe substantial advantages for the explicit understandingof genetics and genomics [5] Recent breakthrough in thesequencing technologies and the availability of tools improvethe accuracy of de novo genome sequencing Unveiling thegenome information gives us an invaluable insight into theepigenetic characteristics [6] Genes responsible for traitsof agronomic importance are rapidly identified and char-acterized with the forward and reverse genetics studies onmany plants [4] Genome-wide association studies (GWAS)characterize the functional role(s) of gene [5] Genotyping-by-sequencing (GBS) and marker assisted selection (MAS)helps the precise breeding program [4] Genomics provideshuge amount of information in convenient manner for evo-lutional studies Comparative analysis among diverse plantfamilies helps to know about the evolutionary details of thegene(s)plant(s) [7] Candidate gene mapping in one speciesserves as a substrate for comparative analysis of other relatedspecies [5]
Therefore this review will cover the progress of NGS ofimportant commercial and model plants in Rosaceae suchas apple pear strawberry peach sweet cherry apricot androse Brief information about the functional genomics studiesconducted on critical key traits of the above-mentionedplants are also covered in this review
2 Genome Assembly and Annotation
Genome-scale study gives rich candidate genetic resourceto deciphering the functional and regulatory networks forgrowth and development NGS is the perfect platformto know about the genomic information which has wideapplication in crop improvement and evolutionary studiesGenome sequencing details of apple pear strawberry peachand rose have been given in Table 1 Desirable key traits willbe discussed in functional genomics section
21 Apple Apple fruit has higher nutritional values Forseveral centuries humans consumed apple-based beveragessuch as ciders [8] Malus x domestica or M pumila is thewidely growing apple tree Ancestor of domesticated Mdomestica is M sieversii It is originated in Central Asia(Southern China) Wild M pumila tree bearing smallersized fruits is still covered 80 of Tian Shan MountainsMicrosatellite markers study showed that M domestica isgenetically similar to European crabapple M sylvestris thanto the Asian wild appleM sieversii [9 10]
So far three genomes have been released in apple FirstlyVelasco et al (2010) covered 813 (6039Mb) of M xdomestica Borkh ldquoGolden Deliciousrdquo genome In that 57386geneswere identified Almost 674 ofM x domestica genomeconsists of repetitive sequences [11] Secondly Li et al (2016)covered about 90 (6324Mb) of M x domestica BorkhldquoGolden Deliciousrdquo genome A total number of identifiedprotein-coding and noncoding genes were 53922 and 2765respectively [12] Thirdly Daccord et al (2017) assembled
genome ofM x domestica Borkh ldquoGolden Delicious doubled-haploidrdquo line (GDDH13) Estimated genome size of GDDH13is 651Mb from which 6497Mb (998) was assembledHowever only 42140 protein-coding genes and 1965 non-protein coding genes were identified in GDDH13 genome[6] Major burst of transposable elements (TEs) happeningaround 21MYAwas correlatedwith the uplift of theTian Shanmountains as well as the diversification of apple and pear[11] Study on structural and functional evolution of genomecannot be completed without characterizing the TEs Around595 of the GDDH13 genome was covered with the TEelements Most interestingly HODOR (High-Copy GoldenDelicious repeat) TE consensus sequences are present atabout 223 Mb (36 of genome) [6]
22 Pear Pear is one of the most important temperate fruitIt is originated in Western China In spite of thousands ofcultivars based on the habituation Pyrus species are dividedinto two major groups such as Occidental pears or Europeanpears (P communis) and Oriental pears or Asiatic pears(P bretschneideri) [13] Nevertheless commercially importantcultivars were domesticated from the wide range of wildspecies still pear cultivation faces challenges such as suscepti-bility to the pear scab black spot disease self-incompatibilityearly ripening short shelf life firmness sucrose contentgritstone cells color and odor of fruit and inbreedingdepression [14]
Recently 971 of P bretschneideri Rehd (Chinese pear)genome ie 5120Mb (42812 genes) has been annotatedby Wu et al [15] Following it 5773Mb of P communis(European pear) was sequenced It covered around 984 ofgenome containing 43419 genes [16] Pear is phylogeneticallycloser towards the apple [1] Hence higher collinearity wasexisted between the chromosomes of pear and apple Pearand apple divergence could have happened only 54-215MYA [15] Presence of repetitive sequence about 531 in Pbretschneideri [15] and 345 in P communis [16] hamperedthe investigation of uncharacterized regions
23 Strawberry Strawberry comes under the category ofsoft fruit It is widely attracted for its aroma bright redcolor texture and taste Preservedprocessed strawberries arelargely used for ice creams milkshakes chocolates etc It isconsidered to be difficult to propagate
231 Fragaria vesca Fragaria vesca is a diploid speciesgenerally called woodland strawberry It has unique char-acteristics such as day neutrality nonrunning and yellowcolored fruits It is self-compatible and has short generationtime It is indigenous to northern Eurasia andNorth America[17]
Small genome (2400Mb) of strawberry (Fragaria vescaldquoHawaai4rdquo) showed the absence of whole genome duplica-tions Though all members of rosids shared the ancient tripli-cation no evidence of whole genome duplication was foundin F vesca About 998 (2395Mb) of genome was coveredwith identification of 33264 genes [17] Later Darwish et aldone the reference based reannotation and assembly of wood-land strawberry F vesca ldquoYW5AF7rdquo genome [18] Similar
BioMed Research International 3
Table1Genom
esequencingof
impo
rtantcom
mercialplantsbelong
stotheR
osaceaefam
ily
Com
mon
name
Samplen
ame
Chrn
umber
Genom
esize
Coverage()
Platform
Num
bero
fgenes
Repetitive
sequ
ences(Mb)
Reference
Estim
ated
(Mb)
Assembled
(Mb)
Apple
Mallusx
domesticaldquoG
oldenDelicou
srdquo
2n=2
x=34
7423
6039
813
BAC+454
57386
3623
Velascoetal2
010
Mallusx
domesticaldquo
GoldenDelicou
srdquo(H
eterologou
s)7010
6324
902
Illum
ina+
PacB
io53922
3820
Lietal2
016
Mallusx
domesticaldquoG
oldenDelicou
sdo
ubled-haploidrdquo
6510
6497
998
Illum
ina+
PacB
io4214
03722
Daccord
etal2
017
Pear
Pyrusb
retsc
hneid
erildquoDangshansulirdquo
2n=2
x=34
5120
5013
979
BAC-
by-BAC
+Illum
ina
42812
2402
Wuetal2
013
Pyruscom
mun
isldquoBartlettrdquo
6000
5773
962
454
43419
1977
Chagne
etal2
014
Strawberry
FragariavescasspvescaaccHaw
aii4
2n=2
x=14
2400
2395
998
Illum
ina+
454+
SOLiD
33264
498
Shulaeve
tal2010
Fragariaxananassa
ldquoReikourdquo
2n=8
x=56
6920
6977
1008lowast
454+Illum
ina
64947
3283
Hira
kawae
tal2014
Fragaria
iinum
ae
2n=2
x=14
2210
1996
903
26411
632
Fragarianipponica
2080
2065
993
21540
525
Fragarianu
bicola
2020
2037
1008lowast
21053
499
Fragariaorien
talis
3493
2142
613
17239
562
Chinesep
lum
and
Japanese
apric
otPrun
usmum
eldquoMeirdquo
2n=2
x=16
2800
237
846
Illum
ina
3139
01068
Zhangetal2
012
Peach
Prun
uspersica
ldquoLovellrdquov10
2n=2
x=16
2650
2246
847
BAC-
by-BAC
27852
8441
Verdee
tal2013
Prun
uspersica
ldquoLovellrdquov20
2274
858
Illum
ina
26873
-Ve
rdee
tal2017
Sweetcherry
Prun
usavium
ldquoSantonishikirdquo
2n=2
x=16
3800
2724
778
Illum
ina
43349
1194
Shira
sawae
tal2017
Rose
Rosa
chinensis
ldquoOld
Blushrdquo
2n=2
x=14
5600
5030
977
Illum
ina+
PacB
io3637
73415
Raym
ondetal2
018
Rosa
chinensis
ldquoOld
Blushrdquo
(dou
bled
haploid
ndashldquoHapOBrdquo)
5680plusmn
905120
901sim961
Illum
ina+
PacB
io44
481
2796
Saint-Oyant
etal
2018
Rosa
multifl
ora
750
711
948
Illum
ina
67380
4172
Nakam
urae
tal2018
lowastTh
ehighersizeo
fgenom
eassem
bled
than
thee
stimated
couldbe
either
duetolim
itatio
nin
thek
mer
abun
danceanalysisor
duplicationoccurringdu
ringtheg
enom
eassem
blyof
highlyrepetitiver
egion
4 BioMed Research International
to the macrosyntenic relationships between pear and appleFragaria shared the synteny with Prunus Lesser genome sizeof F vesca could be mainly due to the lack of highly abundantLTR retrotransposons (lt 2100 copies) Based on the obtainedgenome sequences 389 rosaceous conserved orthologous set(RosCOS) markers were developed in Rosaceae [19]
232 Fragaria x ananassa F x ananassa is commonlycultivated species that play an important role in the straw-berry production worldwide Interestingly F x ananassa wasreported as an accidental hybrid rose in France during mid-1700 between F chiloensis (Chile) and F virginiana (NorthAmerican cultivar) [17]
Genome size of this octoploid species F x ananassawas estimated between 708Mb and 720Mb F x ananassashared the genome information with wild diploids such asF iinumae F nipponica F nubicola and F orientalis andtheir genome size is 221Mb 208Mb 202Mb and 3493MbrespectivelyThe octaploid genome F x ananassawas assem-bled about 6977Mb and its wild relatives are as follows Fiinumae 1996 Mb (903) F nipponica 2064Mb (992) Fnubicola 2036Mb and F orientalis 2142 Mb (613) [20]In total the number of genes identified from F x ananassawas 230838 Protein-coding genes identified in wild relativesare 76760 in F iinumae 87803 in F nipponica 85062 inF nubicola and 99674 in F orientalis About 471 (3282Mb) of F x ananassa genome consists of repeats In case ofwild relatives 317 (633Mb) in F iinumae 255 (526Mb)in F nipponica 245 (499Mb) in F nubicola and 263(562Mb) in F orientalis are repeat regions in genome [20]
24 Prunus Prunus fruit has attractive bright shiny skincolor subtle flavor and sweetness It has long generation timeand bigger plant size It needs 3-5 years for floweringfruitproduction from planting Processed cherry product is soldworldwide
241 Chinese Plum and Japanese Apricot (Prunus mume)Prunus mume is the first plant in Prunoideae subfamilyto be sequenced Domestication of P mume could havestarted 3000 years ago in China [21] This woody perennialis considered as the first tree to be bloomed during thetransition from winter to spring at lesser than 0∘C [22]
Out of 280Mb of the genome size 2370Mb (846)was sequenced Totally 31390 protein-coding genes werecharacterized in the P mume Genome of P mume pro-vides information about the 1154 candidate genes involvedin flower aroma flowering time and disease resistanceAssembled genome contains 1068Mb (450) of repetitivesequences Investigation of P mume genome with the Vitisvinifera paleohexaploid ancestor showed that 27819 genemodels aligned with its seven ancestral chromosomes It isnoteworthy that 2772 orthologsrsquo (781) collinearity blockswere present in the P mume genome (Table 1) Comparativeanalysis of P mume chromosome with the Rosaceae ancestralchromosome showed that 4 5 and 7 chromosomes of Pmume does not undergo any changes and they are directRosaceae ancient chromosomes such as III VII and VIrespectively [23]
242 Peach (Prunus persica) Peach is one of great fruitthat provides vitamins minerals fiber and antioxidant com-pounds Peach fruit is also called nectarine due to smoothskin without fuzz or short hairs Selection and domesticationof peach could have started in Yangzi River valley Chinaaround 7500 years ago [24]
Whole genome analysis of P persica L ldquoLovellrdquo covered2246Mb (847) of genome (estimated total size 265Mb)and represented 27852 protein-coding genes Repetitivesequences present in peach were estimated as 8441Mb(3714) which is lesser than the apple (424) and grape(445) 6726Mb (2960) 2056 Mb (905) and 1714Mb(754) appeared as TEs DNA transposons and unclassifiedrepeats respectively [25] Recently P persica ldquoLovellrdquo doublehaploid genome version 20 was released with deep rese-quencing approach Assembled genome of 2274Mb (858)contains 26873 genes [26]
243 Sweet Cherry (Prunus avium) Prunus avium generallycalled sweet cherry is an important drupe fruit in the Rosaceafamily Sweet cherry is used for human consumption andwildcherry trees for wood which is also called mazzards Sweetcherry and sour cherry are the most commercial and ediblecrops in Prunus genus [27]
Genome size of P avium is about approximately 350MbShirasawa et al (2017) assembled about 778 (2724Mb) ofthe P avium ldquoSatonishikirdquo About 438 (1194Mb) of the Pavium genome were covered with the repetitive sequencesAmong the 1194Mb of repeats 851Mb of repeats are uniqueto P avium ldquoSatonishikirdquo Identified genes clustered with theP persica P mume M domestica and F vesca 75627 genesclusters are formed 3459 clusters (4535 genes) fromP aviumare present in all the investigated species and 16151 clusters(21642 genes) were found only in the P avium with theabsence of 869 clusters [28]
25 Rose Roses are one of the most essential ornamentalplants worldwide Ornamental value of rose enjoyed sincethe dawn of civilization Cultivation of roses traced back to3000 years ago It consists of 200 species and most of themare polyploid It has also been cultivated for its cosmeticvalues such as perfumes and antiques and also some of thephytochemicals of roses have high therapeutic values Rosehips can be used to cure osteoarthritis [29]
251 Rosa chinensis Rosa chinensis is one of the importantpot-type rose cultivars Recently Raymond et al (2018)sequenced the whole genome of R chinensis ldquoOld Blushrdquoand resequenced the major genotypes contributed for rosedomestication Totally 503Mb (977) of the genome wasassembled Genome results comprised 36377 protein-codinggenes 3971 long noncoding RNAs and 207 miRNAs In thegenome TEs were present about 679 From that 506were identified as long-terminal-repeat retrotransposons[30] From the doubled-haploid rose line of R chinensisldquoOld Blushrdquo (ldquoHapOBrdquo) about 901 to 961 (512Mb) ofgenomewas assembled About 466 Mbwas anchored to sevenpseudo-chromosomes and the remaining were assignedto the chromosome 0 (Chr0) Totally 44481 genes were
BioMed Research International 5
identified including 39669 protein-coding and 4812 noncod-ing genes Repeats covered about 2796Mb of genome [31]Rosa and Fragaria genomes shared the eight chromosomesof ancestral Rosaceae with one chromosome fission and twofusions Divergence of Rosa Fragaria and Rubus could haveoccurred within a short period [30] Synteny analysis showedthat chromosomes 1 4 5 6 and 7 of R chinensis havehigher collinearity with chromosomes 7 4 3 2 and 5 of Fvesca Interestingly chromosomes 2 and 3 of R chinensisweredetected as reciprocal translocation with chromosomes 6 and1 of F vesca [31]
252 Rosa multiflora Rosa multiflora is a five-petal plantbelongs to the section Synstylae It is native to the easternAsian regions [32] R multiflora was used for breedingpurpose to the modern roses Especially its resistance locus(Rdr1) tolerance against powdery mildew was introgressedwith the R hybrida [33]
Genome size of R multiflora was estimated as 750Mband about 711Mb was sequenced Assembled genome wascharacterized with 67380 genes (54893 complete genesand 12487 partial genes) Repeat regions covered 564(4172Mb) of assembled genome Out of 18956 gene clustersin R multiflora 1287 904 and 241 clusters were shared withthe F vesca P persica and M x domestica respectively Rmultiflora shared more number of gene clusters with theF vesca than the other two plants of Rosaceae Howeverunique gene clusters and genes of R multiflora are 25 (3482of R multiflora and 1397 of F vesca) and 33 (14663 of Rmultiflora and 4482 of F vesca) times higher than the F vescarespectively [34]
3 Functional Genomics
31 Fruit Development and Sucrose Metabolism in ApplePome is a unique nature of false fruit formation from thebasal part of sepals and receptacles Velasco et al (2010)suggest that pome could have evolved recently from Maleaespecific WGD which could be a major factor contributing toapple development and its specificity [11] Genes encodingfor like-hetero chromatin protein 1 (LHP1) such asMdLHP1aand MdLHP1b regulate the flowering time of apple [35]Flowering locus T1 (MdFT1) can promote flowering whereasterminal flower (MdTFL1 and MdTFL2) expressed in thevegetative part could repress flowering and maintains thevegetative meristem identity [36] Soon after fertilizationhigher expression of two cyclin-dependent kinase (CDK)bgenes and one cyclin-dependent kinase regulatory subunit(CKS) 1 indicates the active cell division of fruits [37] Tran-scription factors such asAgamous (AG) Fruitfull (FUL) AG-like (AGL)1AGL5 Spatula (SPT) Crabs Claw (CRC) andEttin (ETT) regulate the carpel identity and differentiation[38] Microarray data on apple reported that SPT ETTAuxinResponse Factor (ARF) 3 FULAGL8 and CRC transcriptswere abundant during the fruit enlargement stage Howevermost of their expressions are downregulated in cell divisionstage [39] In apple fruit development-related gene familiessuch asMADS-box genes carbohydrate metabolism sorbitolassimilation and transportation were expanded more than
the cucumber soybean poplar A thaliana grape riceBrachypodium sorghum and maize [11] Expression of 120572-expansin (120572-EXP)was detected only during the cell expansionphase of apple [39] MdMADS21 and MdMADS22 orthol-ogous to FUL-like genes in A thaliana were progressivelyinvolved in the fruit developmental process Among twocandidate genes MdMADS21 was closely associated withfruit flesh firmness [40] ARF106 gene expressed duringcell division and cell expansion stages is consistent with apotential role in the control of fruit size [41] Methylation ofDNAplays an essential role in the fruit size [12] Comparativestudy between the bigger size apple (Golden Delicious) andsmaller size apple (GDDH18) showed that twenty-two genesfound as responsible for small size have lesser methylation inthe promoter region [6]
After pollination the small amount of starch present inthe floral buds starts to metabolize Conversion of carbonto sucrose was mediated by the tonoplast monosaccharidetransporters (TMTs) MdTMT1 and MdTMT2 Expansion offruit cells is associated with the starch accumulation Higherexpression of sorbitol dehydrogenase (SHD) cell wall invertase(CIN) neutral invertase (NIN) sucrose synthase (SS) fruc-tokinase (FRK) and hexokinase (HK) indicates the metabo-lization of sorbitol and sucrose [42] In the early period ofcell expansion starch accumulation was higher and it startsto decline in the later phase [11] Transcript of SS genes inapple is correlated with the starch accumulation [39] Sorbitoldehydrogenase (SDH) converts carbohydrate into fructoseNine SDH genes were identified in apple fruit [43] In youngfruit MdSDH1 expression was higher than in mature fruit[42] Other genes significantly upregulated during ripeningstage are isopentenyl pyrophosphate (IPP) isomerase catalase(CAT) histone 2B (H2B) and the ripening-inhibitor (RIN)MADS-box gene [39] During the ripening process a decreaseof starch synthesis is vice versa with the sugar level [44]Expression profiles of sucrose-phosphatase phosphatase (SPP)and sucrose-phosphate synthase (SPS) were active in the ripen-ing stage [42] suggesting that these enzymesmay be involvedin starch degradation pathway Polygalacturonase 1 (MdPG1)and aminocyclopropane-1-carboxylate oxidase (MdACO1)were involved in the fruit softening and ethylene biosynthesisin apple respectively [45] Decrease in the expression ofPG1 alters the firmness tensile strength and water loss inapple M x domestica fruit [46] MeanwhileMdFT1MdACS1(1-aminocyclopropane-1-carboxylic acid synthase) MdACO1and MdExp7 are regulating the fruit softening Amongthem MdExp7 and MdACO1 control firmness in apple [45]Gene coding for MYB TF in apple MdMyb1 increases theanthocyanin content and is responsible for the red skin color[47] Acidity in apple is due to the malic acid and mamarecessive gene is responsible for low acidity [48]
In apple fruit size sugar content and palatability areessential qualities determining its marketability Knowledgeof genes governing the fruit quality could be essential forscreening better linesgenotypes for breeding
32 Lignin Metabolism and Stone Cell Formation in PearStone cell content is the main quality determinant of pearfruit Deposition of lignin on the primary cell wall of
6 BioMed Research International
Lignin synthesis
Branchy sclereids
Stone cells
HCT
LIMMYB
PbCAD2
PbCCR2
PbCCR1
PbCCR3
CCOMTC3H
NAC (NAM ATAF12 and CUC2)
Figure 1 Simple heuristic representation of genestranscription factors involved in lignin synthesis and stone cell formation in pearfruit Pb Pyrus bretschneideri hydroxycinnamoyl transferase HCT p-coumaroyl-shikimatequinate 31015840-hydroxylases C31015840H caffeoyl-CoA O-methyltransferase CCOMT NAM ATAF12 and CUC2 NAC Lin11Isl1Mec3 LIM myeloblastosis MYB cinnamyl alcohol dehydrogenaseCAD and cinnamoyl-CoA reductase CCR Red colored dots represent the stone cells
parenchyma cell followed by the secondary sedimentation ona sclerenchyma cell forms the stone cells Majority of stonecells present in pear is branchy sclereids comprised lignin andcellulose Lignins are synthesized by twoways one starts withp-coumaric acid and second with phenylalanine precursorto cinnamic acid and then p-coumaric acid Other forms oflignin monomers are caffeic acid ferulic acid 5-hydroxy-ferulic acid and sinapinic acid [49ndash51] Finallymonomers arepolymerized to form lignin products Monomers of lignin arecategorized into three types syringly lignin (S-lignin) guaia-cyl lignin (G-lignin) and hydroxyphenyl lignin (H-lignin)From the gnome analysis a total of 66 lignin synthesis-related gene families were characterized in P bretschneideriIt signifies the high demand for lignin synthesis in pear [15]In ldquoDangshan Surdquo pulp milled wood lignin was identifiedas guaiacyl-syringyl-lignin It was observed that ldquoDangshanSurdquo lignin possesses more guaiacyl units than the syringylunits [49] Hydroxycinnamoyl transferases (HCT) play asignificant role in the lignin synthesis [52] Accumulation ofG-lignin and S-lignin is interrelated with theHCT expressionespecially at early fruit developmental stage [15]
Cinnamoyl-CoA reductase (CCR) and cinnamyl alco-hol dehydrogenase (CAD) belonging to medium-or-short-chain dehydrogenasereductase are key enzymes for ligninmonomer synthesis [53] Totally 31 CCRs and 26 CADsgenes were identified in P bretschneideri ldquoDangshan Surdquo Allmembers of CCR and CAD identified in P bretschneideri arenot involved in the lignin biosynthesis [54] Among them
PbCAD2 PbCCR1 PbCCR2 and PbCCR3 were identified toparticipate in the lignin synthesis of stone cells [15] NAC(NAM ATAF12 and CUC2) and LIM (Lin11Isl1Mec3) arean important TF influencing the lignin pathway [55 56]Mostof theCCR andCADmembers present in the pear possess SPL(squamosal promoter binding-like) light-responsive elementon their upstream Functions of PbCCR and PbCAD arerelated to the light signaling Presence of MYB-binding ACcis elements in some promoter of the PbCCRs suggestedthat phenylpropanoid metabolism of lignin synthesis wasregulated by MYB transcription factors Similarly TGACG-motif on some PbCCRs and all PbCADrsquos promoter regionsrevealed their involvement in the abscisic acid jasmonicacid andmethyl jasmonic acidmetabolism [15]The pictorialillustration of genesTFs required for the lignin synthesis aswell as stone cell formation is mentioned in Figure 1
There are many internal and external factors involved inthe stone cell formation of pear Identification of candidategenes of lignin biosynthesis and stone cell formation willbe very much useful to improve the cultural practices forproducing pear fruits with different palatable level of stonecells
33 Fruit Aroma and Softness in Strawberry Strawberry iswidely appreciated for its delicate flavor aroma and nutri-tional value Aroma of strawberry is due to esters alcoholsaldehydes and sulfur compounds Hundreds of volatile estershave been correlated with strawberry ripening and aroma
BioMed Research International 7
[57] Volatile esters are the major constituents of floral scentWild species such as F vesca and F virginiana have muchstronger aroma than the cultivated types Compared to theregular octoploid strawberry unique phenolic compoundswere found inF vesca fruits such as taxifolin 3-O-arabinosideand peonidin 3-O-malonylglucoside [58] Pinene synthase(PINS) is primarily expressed in wild strawberry whileinsertional mutation reduced its expression in cultivatedspecies F vesca contains high amounts of ethyl-acetate andlower methyl-butyrate ethyl-butyrate and furanone levels Fnilgerrensis possesses higher ethyl-acetate and furanone butlower methyl-butyrate and ethyl-butyrate Hybrids betweenF vesca and F ananassa have intermediate contents of fra-grance and aroma related compounds while crosses betweenF nilgerrensis and F ananassa more closely resemble Fnilgerrensis [17] Volatile compounds found to be responsiblefor general strawberry smell are 2 5-dimethyl-4-hydroxy-3(2H)-furanone linalool and ethyl hexanoate Neverthelessethyl butanoate methyl butanoate 120574-decalactone and 2-heptanone are represented as cultivar specific aroma com-pounds [59] O-methyltransferase of strawberry (FaOMT) isvital for the biosynthesis of vanillin and furaneol [60]Alcoholacyltransferase (AATs) in strawberry (SAAT) is involved inthe last step of volatile esters synthesis and vital for flavorbiogenesis in ripening fruit SAAT catalyzes esterificationof an acyl moiety from actyl-CoA to alcohol [61] Straw-berry quinone oxidoreductase (FaQR) is required for thebiosynthesis of furaneol Furaneol and its methoxy derivative(methoxyfuraneol and mesifuran) are catalyzed by OMT Allthree furaneol compounds are highly accumulated duringfruit ripening stage [62] Though two types of pyruvatedecarboxylase (PDC) were identified in strawberry onlyFaPDC1 was induced during fruit ripening [63]
Strawberry is highly perishable even with controlledatmospheric storage Higher proportion of fruit last occurreddue to its softness and sensitivity to fungal disease Redcolored strawberry showed the higher level of anthocyanin-related transcripts [64] FcMYB1 could regulate branching-point of the anthocyaninproanthocyanidin biosynthesisFaWRKY1 mediate defense response and FaPE1 encodedfor pectin methyl esterase are conferred at least with apartial resistance of ripened fruit against Botrytis cinerea[65 66] Polygalacturonase 1 of F x ananassa (FaPG1) iscritical for fruit softening [67] In strawberry fruits beta-D-glucosyltransferase (FaGT) correlated with the relevantphenylpropanoid glucosides [68]D-xylose reductase (FaXyl1)and beta-xylosidase activity were higher in ldquoToyonakardquo (soft)than in the ldquoCamarosardquo (firm) showing the correlationbetween FaXyl1 expression and fruit softening [69] Fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase) is involvedin the firmness and postharvest life [70] A lesser activity ofbeta-galactosidase (120573Gal) and 120573Xyl activity were correlatedwith decreased fruit firmness in F chiloensis and F timesananassa respectively [71] Expression of FaCCR is higherin soft fruit cultivar (Gorella) whereas FaCAD is higher infirm fruit cultivar (Holiday) [72] Expression of five expansingenes (FaEXP1 FaEXP2 FaEXP4 FaEXP5 and FaEXP6) wasstudied in cultivars with different firmness ldquoSelvardquo (hard)ldquoCamarosardquo (medium) and ldquoToyonakardquo (soft) Higher level
of FaEXP1 FaEXP2 and FaEXP5 expression was foundin fruit with less firmness (ldquoToyonakardquo) than the othertwo cultivars (ldquoSelvardquo and ldquoCamarosardquo) Fruit firmnessis identified to be associated with pectate lyase (FaPel1)identified Expansin activity was characterized by cell wallmodification [73] Polysaccharides were modified by fivedifferent genes such as FasPG FaPG-like FaPel1 FaPel2 andFaEXP2 [74] Sorbitol dehydrogenase (FaSDH) and sorbitol-6-phosphate dehydrogenase (FaS6PDH) genes are involved withthe sorbitol synthesis in leaves fruits and shoot tips [75]SEPALLATA (SEP)4-like gene FaMADS9 is responsible forthe fruit ripening [76]
Apart from the aesthetic and taste mechanisms of flower-ing and its response to the light signaling in strawberry needto be studied in detail Cultivars with continuous floweringand growing underminimal light energy are beneficial for thestrawberry growers as most of the commercial cultivation iscarried out in the controlled greenhouse
34 Early Blooming and Fruit Ripening in Prunus Prunusis the first plant to bloom in later winterearly spring Soit is the best model plant to study early flowering as wellas chilling tolerance Dehydrins are known as 2 or D-11family late-embryogenesis-abundant (LEA) proteins Theyplay a vital role in plant growth and cold tolerance [77] InP mume 30 LEA genes were characterized and classifiedinto eight groups LEA1 LEA2 LEA3 LEA4 LEA5 PvLEA18dehydrin and seed maturation protein Out of 30 identifiedgenes 22 were expressed in flowers and 19 were inducedby abscisic acid (ABA) treatments [78] Molecular cloningof PmLEA8 PmLEA10 PmLEA19 PmLEA20 and PmLEA29showed that except PmLEA8 all other genes enhancedthe freezing-tolerance Interestingly among all cold-resistantLEA genemembers studied only PmLEA19were upregulatedfour timeswhen the branches of Pmumewere exposed to 4∘C[79]Downregulation inPmume dormancy associatedMADS(PmDAM) 4 PmDAM5 and PmDAM6 expression releasesthe endodormancy [80] Among the six DAM genes exceptPmDAM3 all other genes are responsive to the photoperiodand seasonal (cold) responses [81] In P persica from six iden-tified DAM genes PpDAM5 and PpDAM6 were character-ized to be involved in the lateral bud dormancy breakage [82]DAM5 and DAM6 were identified as homologous to ShortVegetative Phase (SVP)AGL 24 in A thaliana Both SVPand AGL-24 are required for floral meristem identity [83]AGL24 is well known for promoting early flowering and floraltransition in plants [58] Transcriptome analysis betweencold sensitive (ldquoMorettinirdquo) and cold tolerant (ldquoRoyal Gloryrdquo)cultivars in P persica showed that 120573-D-xylosidase (BXL)and pathogen-related protein 4b (PR-4B) were significantlyexpressed only in resistant variety [84] Other candidategenes identified as required to control flowering time aresuppressor of phyA (SPA) COP1 interacting protein8 (CIP8)phytochrome A (phyA) and phytochrome interacting factor 3(PIF3) [85] Figure 2 demonstrates the important key genesinvolved in cold tolerance early blooming and floweringtime control of P mume Higher number of aesthetic prop-erties related genes such as benzyl alcohol acetyltransferase(BEAT) (34) are identified in P mume Only 16 in Malus x
8 BioMed Research International
PmLEA19 PmDAM4 PmDAM5 and PmDAM6
SPA CIP8 phyA and PIF3BXL and PR-4B
Cold toler
ance
Cold tolerance
Control flowering time
Dorman
cy re
lease
Figure 2 Factors involved in the early blooming of Chinese plumJapanese apricot Prunus meme Pm late-embryogenesis-abundant LEAdormancy associated MADS DAM 120573-D-xylosidase BXL pathogen-related protein 4b PR-4B suppressor of phyA SPA COP1 interactingprotein8 CIP8 phytochrome A phyA and phytochrome interacting factor3 PIF3 The lower arrow represents downregulation
domestica 14 in F vesca 4 inVitis vinifera 17 in P trichocarpaand 3 inA thaliana of BEAT genes were identifiedThereforein P mume BEAT genes are considered as key factor todetermine its exclusive floral fragrance [23]
In Prunus UDP-glucose-flavonoid-3-O-glucosyltransfer-ase (UFGT) expression was higher during the initial periodand it is reduced on the developmental process Duringthe ripening processMYB10 MYB123 and basic-helix-loop-helix (bHLH3)were upregulatedwhereasMYB16 andMYB111were downregulated Higher anthocyanin and Proantho-cyanidin levels were correlatedwith theMYB10 andMYBPA1respectively Stimulation of TFs is responsive for the devel-opment and external stimuli [86] Gene encoding ethylene-responsive transcription factor (ERF)4 is necessary for the fruitmaturity [87] Though 74 EFR genes were predicted in thepeach genome only one copy of ERF4 has existed ThereforeERF4 is vital to control the fruit maturity and ripening inpeach [85] An initial stage of fruit has higher aldehyde andalcohol production whereas later stages have lesser contentwhich is correlated with the ester production Abundance ofalcohol dehydrogenase (ADH) and lipoxygenase (LOX) geneis constant in the fruit development stages Expression ofAATwas sharply increased in the later stage of harvest [88] Rapidsoftening of fruits was related to the ethylene productionin P persica It is correlated with expression of PpACS1 (1-aminocyclopropane-1-carboxylic acid synthase) [89] Ripenedsweet cherry P avium has unique fragrance In the sweetcherry (ldquoHongdengrdquo ldquoHongyanrdquo and ldquoRainierrdquo) 97 volatilecompounds were identified Alcohols and terpenes were thepredominant components of bound volatiles Benzyl alcoholgeraniol and 2-phenylethanol are the major bound volatileconstituents Free volatile compounds majorly present insweet cherry are hexanal 2-hexenal 2-hexen-1-ol benzyl
alcohol and benzaldehyde Free volatiles are responsible forfloral aroma and bound volatiles involved in fruit freshnessDepending on the level of free and bound volatiles aroma andglycosidically bound compounds aroma and fruit firmnesswere varied between the cultivars of sweet cherry [90]
In Prunus apricot peach sweet cherry and sour cherryare widely used for human consumption Comparativegenomics study between the species offer the candidate geneto produce hybrids with more preferable qualities
35 Blooming and Scent Pathways in Rose Continuous flow-ering (CF)recurrent blooming (RB) genotypes flowers in allfavorable seasons whereas once-flowering (OF) genotypesonly flowers in spring Recurrent blooming is an importanttrait required by breeders R x hybrida ldquoLa Francerdquo was thefirst hybrid combined with the growth vigor of Europeanspecies and recurrent blooming of Chinese species It hasthe complex genetic pool combination of three ancestralgenotypes such as Cinnamomeae Synstylae and ChinensesInsertion of TE in the TFL1 encodes gene Ksncopia (KSN)was found as responsible for the recurrent blooming of ldquoLaFrancerdquo [30] Previously Horibe et al (2013) reported thatKSN gene regulates the CF behavior of R rugosa [91] Wanget al (2012) studied recurrent flowering character and theexpression patterns of TFL1 homologs in R multiflora Rrugosa R chinensis and other speciescultivars Among thethree orthologs RTFL1c was highly expressed at all fourflowering stages in R multiflora and R rugosa (nonrecurrentflowering species) and barely detected in R chinensis (arecurrent flowering species) at any stage Therefore it can beconsidered that lower expression of RTFL1c is required forrecurrent flowering of roses [92] Iwata et al (2012) elucidatethat occurrence of TE insertion and point mutation in the
BioMed Research International 9
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
to the macrosyntenic relationships between pear and appleFragaria shared the synteny with Prunus Lesser genome sizeof F vesca could be mainly due to the lack of highly abundantLTR retrotransposons (lt 2100 copies) Based on the obtainedgenome sequences 389 rosaceous conserved orthologous set(RosCOS) markers were developed in Rosaceae [19]
232 Fragaria x ananassa F x ananassa is commonlycultivated species that play an important role in the straw-berry production worldwide Interestingly F x ananassa wasreported as an accidental hybrid rose in France during mid-1700 between F chiloensis (Chile) and F virginiana (NorthAmerican cultivar) [17]
Genome size of this octoploid species F x ananassawas estimated between 708Mb and 720Mb F x ananassashared the genome information with wild diploids such asF iinumae F nipponica F nubicola and F orientalis andtheir genome size is 221Mb 208Mb 202Mb and 3493MbrespectivelyThe octaploid genome F x ananassawas assem-bled about 6977Mb and its wild relatives are as follows Fiinumae 1996 Mb (903) F nipponica 2064Mb (992) Fnubicola 2036Mb and F orientalis 2142 Mb (613) [20]In total the number of genes identified from F x ananassawas 230838 Protein-coding genes identified in wild relativesare 76760 in F iinumae 87803 in F nipponica 85062 inF nubicola and 99674 in F orientalis About 471 (3282Mb) of F x ananassa genome consists of repeats In case ofwild relatives 317 (633Mb) in F iinumae 255 (526Mb)in F nipponica 245 (499Mb) in F nubicola and 263(562Mb) in F orientalis are repeat regions in genome [20]
24 Prunus Prunus fruit has attractive bright shiny skincolor subtle flavor and sweetness It has long generation timeand bigger plant size It needs 3-5 years for floweringfruitproduction from planting Processed cherry product is soldworldwide
241 Chinese Plum and Japanese Apricot (Prunus mume)Prunus mume is the first plant in Prunoideae subfamilyto be sequenced Domestication of P mume could havestarted 3000 years ago in China [21] This woody perennialis considered as the first tree to be bloomed during thetransition from winter to spring at lesser than 0∘C [22]
Out of 280Mb of the genome size 2370Mb (846)was sequenced Totally 31390 protein-coding genes werecharacterized in the P mume Genome of P mume pro-vides information about the 1154 candidate genes involvedin flower aroma flowering time and disease resistanceAssembled genome contains 1068Mb (450) of repetitivesequences Investigation of P mume genome with the Vitisvinifera paleohexaploid ancestor showed that 27819 genemodels aligned with its seven ancestral chromosomes It isnoteworthy that 2772 orthologsrsquo (781) collinearity blockswere present in the P mume genome (Table 1) Comparativeanalysis of P mume chromosome with the Rosaceae ancestralchromosome showed that 4 5 and 7 chromosomes of Pmume does not undergo any changes and they are directRosaceae ancient chromosomes such as III VII and VIrespectively [23]
242 Peach (Prunus persica) Peach is one of great fruitthat provides vitamins minerals fiber and antioxidant com-pounds Peach fruit is also called nectarine due to smoothskin without fuzz or short hairs Selection and domesticationof peach could have started in Yangzi River valley Chinaaround 7500 years ago [24]
Whole genome analysis of P persica L ldquoLovellrdquo covered2246Mb (847) of genome (estimated total size 265Mb)and represented 27852 protein-coding genes Repetitivesequences present in peach were estimated as 8441Mb(3714) which is lesser than the apple (424) and grape(445) 6726Mb (2960) 2056 Mb (905) and 1714Mb(754) appeared as TEs DNA transposons and unclassifiedrepeats respectively [25] Recently P persica ldquoLovellrdquo doublehaploid genome version 20 was released with deep rese-quencing approach Assembled genome of 2274Mb (858)contains 26873 genes [26]
243 Sweet Cherry (Prunus avium) Prunus avium generallycalled sweet cherry is an important drupe fruit in the Rosaceafamily Sweet cherry is used for human consumption andwildcherry trees for wood which is also called mazzards Sweetcherry and sour cherry are the most commercial and ediblecrops in Prunus genus [27]
Genome size of P avium is about approximately 350MbShirasawa et al (2017) assembled about 778 (2724Mb) ofthe P avium ldquoSatonishikirdquo About 438 (1194Mb) of the Pavium genome were covered with the repetitive sequencesAmong the 1194Mb of repeats 851Mb of repeats are uniqueto P avium ldquoSatonishikirdquo Identified genes clustered with theP persica P mume M domestica and F vesca 75627 genesclusters are formed 3459 clusters (4535 genes) fromP aviumare present in all the investigated species and 16151 clusters(21642 genes) were found only in the P avium with theabsence of 869 clusters [28]
25 Rose Roses are one of the most essential ornamentalplants worldwide Ornamental value of rose enjoyed sincethe dawn of civilization Cultivation of roses traced back to3000 years ago It consists of 200 species and most of themare polyploid It has also been cultivated for its cosmeticvalues such as perfumes and antiques and also some of thephytochemicals of roses have high therapeutic values Rosehips can be used to cure osteoarthritis [29]
251 Rosa chinensis Rosa chinensis is one of the importantpot-type rose cultivars Recently Raymond et al (2018)sequenced the whole genome of R chinensis ldquoOld Blushrdquoand resequenced the major genotypes contributed for rosedomestication Totally 503Mb (977) of the genome wasassembled Genome results comprised 36377 protein-codinggenes 3971 long noncoding RNAs and 207 miRNAs In thegenome TEs were present about 679 From that 506were identified as long-terminal-repeat retrotransposons[30] From the doubled-haploid rose line of R chinensisldquoOld Blushrdquo (ldquoHapOBrdquo) about 901 to 961 (512Mb) ofgenomewas assembled About 466 Mbwas anchored to sevenpseudo-chromosomes and the remaining were assignedto the chromosome 0 (Chr0) Totally 44481 genes were
BioMed Research International 5
identified including 39669 protein-coding and 4812 noncod-ing genes Repeats covered about 2796Mb of genome [31]Rosa and Fragaria genomes shared the eight chromosomesof ancestral Rosaceae with one chromosome fission and twofusions Divergence of Rosa Fragaria and Rubus could haveoccurred within a short period [30] Synteny analysis showedthat chromosomes 1 4 5 6 and 7 of R chinensis havehigher collinearity with chromosomes 7 4 3 2 and 5 of Fvesca Interestingly chromosomes 2 and 3 of R chinensisweredetected as reciprocal translocation with chromosomes 6 and1 of F vesca [31]
252 Rosa multiflora Rosa multiflora is a five-petal plantbelongs to the section Synstylae It is native to the easternAsian regions [32] R multiflora was used for breedingpurpose to the modern roses Especially its resistance locus(Rdr1) tolerance against powdery mildew was introgressedwith the R hybrida [33]
Genome size of R multiflora was estimated as 750Mband about 711Mb was sequenced Assembled genome wascharacterized with 67380 genes (54893 complete genesand 12487 partial genes) Repeat regions covered 564(4172Mb) of assembled genome Out of 18956 gene clustersin R multiflora 1287 904 and 241 clusters were shared withthe F vesca P persica and M x domestica respectively Rmultiflora shared more number of gene clusters with theF vesca than the other two plants of Rosaceae Howeverunique gene clusters and genes of R multiflora are 25 (3482of R multiflora and 1397 of F vesca) and 33 (14663 of Rmultiflora and 4482 of F vesca) times higher than the F vescarespectively [34]
3 Functional Genomics
31 Fruit Development and Sucrose Metabolism in ApplePome is a unique nature of false fruit formation from thebasal part of sepals and receptacles Velasco et al (2010)suggest that pome could have evolved recently from Maleaespecific WGD which could be a major factor contributing toapple development and its specificity [11] Genes encodingfor like-hetero chromatin protein 1 (LHP1) such asMdLHP1aand MdLHP1b regulate the flowering time of apple [35]Flowering locus T1 (MdFT1) can promote flowering whereasterminal flower (MdTFL1 and MdTFL2) expressed in thevegetative part could repress flowering and maintains thevegetative meristem identity [36] Soon after fertilizationhigher expression of two cyclin-dependent kinase (CDK)bgenes and one cyclin-dependent kinase regulatory subunit(CKS) 1 indicates the active cell division of fruits [37] Tran-scription factors such asAgamous (AG) Fruitfull (FUL) AG-like (AGL)1AGL5 Spatula (SPT) Crabs Claw (CRC) andEttin (ETT) regulate the carpel identity and differentiation[38] Microarray data on apple reported that SPT ETTAuxinResponse Factor (ARF) 3 FULAGL8 and CRC transcriptswere abundant during the fruit enlargement stage Howevermost of their expressions are downregulated in cell divisionstage [39] In apple fruit development-related gene familiessuch asMADS-box genes carbohydrate metabolism sorbitolassimilation and transportation were expanded more than
the cucumber soybean poplar A thaliana grape riceBrachypodium sorghum and maize [11] Expression of 120572-expansin (120572-EXP)was detected only during the cell expansionphase of apple [39] MdMADS21 and MdMADS22 orthol-ogous to FUL-like genes in A thaliana were progressivelyinvolved in the fruit developmental process Among twocandidate genes MdMADS21 was closely associated withfruit flesh firmness [40] ARF106 gene expressed duringcell division and cell expansion stages is consistent with apotential role in the control of fruit size [41] Methylation ofDNAplays an essential role in the fruit size [12] Comparativestudy between the bigger size apple (Golden Delicious) andsmaller size apple (GDDH18) showed that twenty-two genesfound as responsible for small size have lesser methylation inthe promoter region [6]
After pollination the small amount of starch present inthe floral buds starts to metabolize Conversion of carbonto sucrose was mediated by the tonoplast monosaccharidetransporters (TMTs) MdTMT1 and MdTMT2 Expansion offruit cells is associated with the starch accumulation Higherexpression of sorbitol dehydrogenase (SHD) cell wall invertase(CIN) neutral invertase (NIN) sucrose synthase (SS) fruc-tokinase (FRK) and hexokinase (HK) indicates the metabo-lization of sorbitol and sucrose [42] In the early period ofcell expansion starch accumulation was higher and it startsto decline in the later phase [11] Transcript of SS genes inapple is correlated with the starch accumulation [39] Sorbitoldehydrogenase (SDH) converts carbohydrate into fructoseNine SDH genes were identified in apple fruit [43] In youngfruit MdSDH1 expression was higher than in mature fruit[42] Other genes significantly upregulated during ripeningstage are isopentenyl pyrophosphate (IPP) isomerase catalase(CAT) histone 2B (H2B) and the ripening-inhibitor (RIN)MADS-box gene [39] During the ripening process a decreaseof starch synthesis is vice versa with the sugar level [44]Expression profiles of sucrose-phosphatase phosphatase (SPP)and sucrose-phosphate synthase (SPS) were active in the ripen-ing stage [42] suggesting that these enzymesmay be involvedin starch degradation pathway Polygalacturonase 1 (MdPG1)and aminocyclopropane-1-carboxylate oxidase (MdACO1)were involved in the fruit softening and ethylene biosynthesisin apple respectively [45] Decrease in the expression ofPG1 alters the firmness tensile strength and water loss inapple M x domestica fruit [46] MeanwhileMdFT1MdACS1(1-aminocyclopropane-1-carboxylic acid synthase) MdACO1and MdExp7 are regulating the fruit softening Amongthem MdExp7 and MdACO1 control firmness in apple [45]Gene coding for MYB TF in apple MdMyb1 increases theanthocyanin content and is responsible for the red skin color[47] Acidity in apple is due to the malic acid and mamarecessive gene is responsible for low acidity [48]
In apple fruit size sugar content and palatability areessential qualities determining its marketability Knowledgeof genes governing the fruit quality could be essential forscreening better linesgenotypes for breeding
32 Lignin Metabolism and Stone Cell Formation in PearStone cell content is the main quality determinant of pearfruit Deposition of lignin on the primary cell wall of
6 BioMed Research International
Lignin synthesis
Branchy sclereids
Stone cells
HCT
LIMMYB
PbCAD2
PbCCR2
PbCCR1
PbCCR3
CCOMTC3H
NAC (NAM ATAF12 and CUC2)
Figure 1 Simple heuristic representation of genestranscription factors involved in lignin synthesis and stone cell formation in pearfruit Pb Pyrus bretschneideri hydroxycinnamoyl transferase HCT p-coumaroyl-shikimatequinate 31015840-hydroxylases C31015840H caffeoyl-CoA O-methyltransferase CCOMT NAM ATAF12 and CUC2 NAC Lin11Isl1Mec3 LIM myeloblastosis MYB cinnamyl alcohol dehydrogenaseCAD and cinnamoyl-CoA reductase CCR Red colored dots represent the stone cells
parenchyma cell followed by the secondary sedimentation ona sclerenchyma cell forms the stone cells Majority of stonecells present in pear is branchy sclereids comprised lignin andcellulose Lignins are synthesized by twoways one starts withp-coumaric acid and second with phenylalanine precursorto cinnamic acid and then p-coumaric acid Other forms oflignin monomers are caffeic acid ferulic acid 5-hydroxy-ferulic acid and sinapinic acid [49ndash51] Finallymonomers arepolymerized to form lignin products Monomers of lignin arecategorized into three types syringly lignin (S-lignin) guaia-cyl lignin (G-lignin) and hydroxyphenyl lignin (H-lignin)From the gnome analysis a total of 66 lignin synthesis-related gene families were characterized in P bretschneideriIt signifies the high demand for lignin synthesis in pear [15]In ldquoDangshan Surdquo pulp milled wood lignin was identifiedas guaiacyl-syringyl-lignin It was observed that ldquoDangshanSurdquo lignin possesses more guaiacyl units than the syringylunits [49] Hydroxycinnamoyl transferases (HCT) play asignificant role in the lignin synthesis [52] Accumulation ofG-lignin and S-lignin is interrelated with theHCT expressionespecially at early fruit developmental stage [15]
Cinnamoyl-CoA reductase (CCR) and cinnamyl alco-hol dehydrogenase (CAD) belonging to medium-or-short-chain dehydrogenasereductase are key enzymes for ligninmonomer synthesis [53] Totally 31 CCRs and 26 CADsgenes were identified in P bretschneideri ldquoDangshan Surdquo Allmembers of CCR and CAD identified in P bretschneideri arenot involved in the lignin biosynthesis [54] Among them
PbCAD2 PbCCR1 PbCCR2 and PbCCR3 were identified toparticipate in the lignin synthesis of stone cells [15] NAC(NAM ATAF12 and CUC2) and LIM (Lin11Isl1Mec3) arean important TF influencing the lignin pathway [55 56]Mostof theCCR andCADmembers present in the pear possess SPL(squamosal promoter binding-like) light-responsive elementon their upstream Functions of PbCCR and PbCAD arerelated to the light signaling Presence of MYB-binding ACcis elements in some promoter of the PbCCRs suggestedthat phenylpropanoid metabolism of lignin synthesis wasregulated by MYB transcription factors Similarly TGACG-motif on some PbCCRs and all PbCADrsquos promoter regionsrevealed their involvement in the abscisic acid jasmonicacid andmethyl jasmonic acidmetabolism [15]The pictorialillustration of genesTFs required for the lignin synthesis aswell as stone cell formation is mentioned in Figure 1
There are many internal and external factors involved inthe stone cell formation of pear Identification of candidategenes of lignin biosynthesis and stone cell formation willbe very much useful to improve the cultural practices forproducing pear fruits with different palatable level of stonecells
33 Fruit Aroma and Softness in Strawberry Strawberry iswidely appreciated for its delicate flavor aroma and nutri-tional value Aroma of strawberry is due to esters alcoholsaldehydes and sulfur compounds Hundreds of volatile estershave been correlated with strawberry ripening and aroma
BioMed Research International 7
[57] Volatile esters are the major constituents of floral scentWild species such as F vesca and F virginiana have muchstronger aroma than the cultivated types Compared to theregular octoploid strawberry unique phenolic compoundswere found inF vesca fruits such as taxifolin 3-O-arabinosideand peonidin 3-O-malonylglucoside [58] Pinene synthase(PINS) is primarily expressed in wild strawberry whileinsertional mutation reduced its expression in cultivatedspecies F vesca contains high amounts of ethyl-acetate andlower methyl-butyrate ethyl-butyrate and furanone levels Fnilgerrensis possesses higher ethyl-acetate and furanone butlower methyl-butyrate and ethyl-butyrate Hybrids betweenF vesca and F ananassa have intermediate contents of fra-grance and aroma related compounds while crosses betweenF nilgerrensis and F ananassa more closely resemble Fnilgerrensis [17] Volatile compounds found to be responsiblefor general strawberry smell are 2 5-dimethyl-4-hydroxy-3(2H)-furanone linalool and ethyl hexanoate Neverthelessethyl butanoate methyl butanoate 120574-decalactone and 2-heptanone are represented as cultivar specific aroma com-pounds [59] O-methyltransferase of strawberry (FaOMT) isvital for the biosynthesis of vanillin and furaneol [60]Alcoholacyltransferase (AATs) in strawberry (SAAT) is involved inthe last step of volatile esters synthesis and vital for flavorbiogenesis in ripening fruit SAAT catalyzes esterificationof an acyl moiety from actyl-CoA to alcohol [61] Straw-berry quinone oxidoreductase (FaQR) is required for thebiosynthesis of furaneol Furaneol and its methoxy derivative(methoxyfuraneol and mesifuran) are catalyzed by OMT Allthree furaneol compounds are highly accumulated duringfruit ripening stage [62] Though two types of pyruvatedecarboxylase (PDC) were identified in strawberry onlyFaPDC1 was induced during fruit ripening [63]
Strawberry is highly perishable even with controlledatmospheric storage Higher proportion of fruit last occurreddue to its softness and sensitivity to fungal disease Redcolored strawberry showed the higher level of anthocyanin-related transcripts [64] FcMYB1 could regulate branching-point of the anthocyaninproanthocyanidin biosynthesisFaWRKY1 mediate defense response and FaPE1 encodedfor pectin methyl esterase are conferred at least with apartial resistance of ripened fruit against Botrytis cinerea[65 66] Polygalacturonase 1 of F x ananassa (FaPG1) iscritical for fruit softening [67] In strawberry fruits beta-D-glucosyltransferase (FaGT) correlated with the relevantphenylpropanoid glucosides [68]D-xylose reductase (FaXyl1)and beta-xylosidase activity were higher in ldquoToyonakardquo (soft)than in the ldquoCamarosardquo (firm) showing the correlationbetween FaXyl1 expression and fruit softening [69] Fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase) is involvedin the firmness and postharvest life [70] A lesser activity ofbeta-galactosidase (120573Gal) and 120573Xyl activity were correlatedwith decreased fruit firmness in F chiloensis and F timesananassa respectively [71] Expression of FaCCR is higherin soft fruit cultivar (Gorella) whereas FaCAD is higher infirm fruit cultivar (Holiday) [72] Expression of five expansingenes (FaEXP1 FaEXP2 FaEXP4 FaEXP5 and FaEXP6) wasstudied in cultivars with different firmness ldquoSelvardquo (hard)ldquoCamarosardquo (medium) and ldquoToyonakardquo (soft) Higher level
of FaEXP1 FaEXP2 and FaEXP5 expression was foundin fruit with less firmness (ldquoToyonakardquo) than the othertwo cultivars (ldquoSelvardquo and ldquoCamarosardquo) Fruit firmnessis identified to be associated with pectate lyase (FaPel1)identified Expansin activity was characterized by cell wallmodification [73] Polysaccharides were modified by fivedifferent genes such as FasPG FaPG-like FaPel1 FaPel2 andFaEXP2 [74] Sorbitol dehydrogenase (FaSDH) and sorbitol-6-phosphate dehydrogenase (FaS6PDH) genes are involved withthe sorbitol synthesis in leaves fruits and shoot tips [75]SEPALLATA (SEP)4-like gene FaMADS9 is responsible forthe fruit ripening [76]
Apart from the aesthetic and taste mechanisms of flower-ing and its response to the light signaling in strawberry needto be studied in detail Cultivars with continuous floweringand growing underminimal light energy are beneficial for thestrawberry growers as most of the commercial cultivation iscarried out in the controlled greenhouse
34 Early Blooming and Fruit Ripening in Prunus Prunusis the first plant to bloom in later winterearly spring Soit is the best model plant to study early flowering as wellas chilling tolerance Dehydrins are known as 2 or D-11family late-embryogenesis-abundant (LEA) proteins Theyplay a vital role in plant growth and cold tolerance [77] InP mume 30 LEA genes were characterized and classifiedinto eight groups LEA1 LEA2 LEA3 LEA4 LEA5 PvLEA18dehydrin and seed maturation protein Out of 30 identifiedgenes 22 were expressed in flowers and 19 were inducedby abscisic acid (ABA) treatments [78] Molecular cloningof PmLEA8 PmLEA10 PmLEA19 PmLEA20 and PmLEA29showed that except PmLEA8 all other genes enhancedthe freezing-tolerance Interestingly among all cold-resistantLEA genemembers studied only PmLEA19were upregulatedfour timeswhen the branches of Pmumewere exposed to 4∘C[79]Downregulation inPmume dormancy associatedMADS(PmDAM) 4 PmDAM5 and PmDAM6 expression releasesthe endodormancy [80] Among the six DAM genes exceptPmDAM3 all other genes are responsive to the photoperiodand seasonal (cold) responses [81] In P persica from six iden-tified DAM genes PpDAM5 and PpDAM6 were character-ized to be involved in the lateral bud dormancy breakage [82]DAM5 and DAM6 were identified as homologous to ShortVegetative Phase (SVP)AGL 24 in A thaliana Both SVPand AGL-24 are required for floral meristem identity [83]AGL24 is well known for promoting early flowering and floraltransition in plants [58] Transcriptome analysis betweencold sensitive (ldquoMorettinirdquo) and cold tolerant (ldquoRoyal Gloryrdquo)cultivars in P persica showed that 120573-D-xylosidase (BXL)and pathogen-related protein 4b (PR-4B) were significantlyexpressed only in resistant variety [84] Other candidategenes identified as required to control flowering time aresuppressor of phyA (SPA) COP1 interacting protein8 (CIP8)phytochrome A (phyA) and phytochrome interacting factor 3(PIF3) [85] Figure 2 demonstrates the important key genesinvolved in cold tolerance early blooming and floweringtime control of P mume Higher number of aesthetic prop-erties related genes such as benzyl alcohol acetyltransferase(BEAT) (34) are identified in P mume Only 16 in Malus x
8 BioMed Research International
PmLEA19 PmDAM4 PmDAM5 and PmDAM6
SPA CIP8 phyA and PIF3BXL and PR-4B
Cold toler
ance
Cold tolerance
Control flowering time
Dorman
cy re
lease
Figure 2 Factors involved in the early blooming of Chinese plumJapanese apricot Prunus meme Pm late-embryogenesis-abundant LEAdormancy associated MADS DAM 120573-D-xylosidase BXL pathogen-related protein 4b PR-4B suppressor of phyA SPA COP1 interactingprotein8 CIP8 phytochrome A phyA and phytochrome interacting factor3 PIF3 The lower arrow represents downregulation
domestica 14 in F vesca 4 inVitis vinifera 17 in P trichocarpaand 3 inA thaliana of BEAT genes were identifiedThereforein P mume BEAT genes are considered as key factor todetermine its exclusive floral fragrance [23]
In Prunus UDP-glucose-flavonoid-3-O-glucosyltransfer-ase (UFGT) expression was higher during the initial periodand it is reduced on the developmental process Duringthe ripening processMYB10 MYB123 and basic-helix-loop-helix (bHLH3)were upregulatedwhereasMYB16 andMYB111were downregulated Higher anthocyanin and Proantho-cyanidin levels were correlatedwith theMYB10 andMYBPA1respectively Stimulation of TFs is responsive for the devel-opment and external stimuli [86] Gene encoding ethylene-responsive transcription factor (ERF)4 is necessary for the fruitmaturity [87] Though 74 EFR genes were predicted in thepeach genome only one copy of ERF4 has existed ThereforeERF4 is vital to control the fruit maturity and ripening inpeach [85] An initial stage of fruit has higher aldehyde andalcohol production whereas later stages have lesser contentwhich is correlated with the ester production Abundance ofalcohol dehydrogenase (ADH) and lipoxygenase (LOX) geneis constant in the fruit development stages Expression ofAATwas sharply increased in the later stage of harvest [88] Rapidsoftening of fruits was related to the ethylene productionin P persica It is correlated with expression of PpACS1 (1-aminocyclopropane-1-carboxylic acid synthase) [89] Ripenedsweet cherry P avium has unique fragrance In the sweetcherry (ldquoHongdengrdquo ldquoHongyanrdquo and ldquoRainierrdquo) 97 volatilecompounds were identified Alcohols and terpenes were thepredominant components of bound volatiles Benzyl alcoholgeraniol and 2-phenylethanol are the major bound volatileconstituents Free volatile compounds majorly present insweet cherry are hexanal 2-hexenal 2-hexen-1-ol benzyl
alcohol and benzaldehyde Free volatiles are responsible forfloral aroma and bound volatiles involved in fruit freshnessDepending on the level of free and bound volatiles aroma andglycosidically bound compounds aroma and fruit firmnesswere varied between the cultivars of sweet cherry [90]
In Prunus apricot peach sweet cherry and sour cherryare widely used for human consumption Comparativegenomics study between the species offer the candidate geneto produce hybrids with more preferable qualities
35 Blooming and Scent Pathways in Rose Continuous flow-ering (CF)recurrent blooming (RB) genotypes flowers in allfavorable seasons whereas once-flowering (OF) genotypesonly flowers in spring Recurrent blooming is an importanttrait required by breeders R x hybrida ldquoLa Francerdquo was thefirst hybrid combined with the growth vigor of Europeanspecies and recurrent blooming of Chinese species It hasthe complex genetic pool combination of three ancestralgenotypes such as Cinnamomeae Synstylae and ChinensesInsertion of TE in the TFL1 encodes gene Ksncopia (KSN)was found as responsible for the recurrent blooming of ldquoLaFrancerdquo [30] Previously Horibe et al (2013) reported thatKSN gene regulates the CF behavior of R rugosa [91] Wanget al (2012) studied recurrent flowering character and theexpression patterns of TFL1 homologs in R multiflora Rrugosa R chinensis and other speciescultivars Among thethree orthologs RTFL1c was highly expressed at all fourflowering stages in R multiflora and R rugosa (nonrecurrentflowering species) and barely detected in R chinensis (arecurrent flowering species) at any stage Therefore it can beconsidered that lower expression of RTFL1c is required forrecurrent flowering of roses [92] Iwata et al (2012) elucidatethat occurrence of TE insertion and point mutation in the
BioMed Research International 9
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
to the macrosyntenic relationships between pear and appleFragaria shared the synteny with Prunus Lesser genome sizeof F vesca could be mainly due to the lack of highly abundantLTR retrotransposons (lt 2100 copies) Based on the obtainedgenome sequences 389 rosaceous conserved orthologous set(RosCOS) markers were developed in Rosaceae [19]
232 Fragaria x ananassa F x ananassa is commonlycultivated species that play an important role in the straw-berry production worldwide Interestingly F x ananassa wasreported as an accidental hybrid rose in France during mid-1700 between F chiloensis (Chile) and F virginiana (NorthAmerican cultivar) [17]
Genome size of this octoploid species F x ananassawas estimated between 708Mb and 720Mb F x ananassashared the genome information with wild diploids such asF iinumae F nipponica F nubicola and F orientalis andtheir genome size is 221Mb 208Mb 202Mb and 3493MbrespectivelyThe octaploid genome F x ananassawas assem-bled about 6977Mb and its wild relatives are as follows Fiinumae 1996 Mb (903) F nipponica 2064Mb (992) Fnubicola 2036Mb and F orientalis 2142 Mb (613) [20]In total the number of genes identified from F x ananassawas 230838 Protein-coding genes identified in wild relativesare 76760 in F iinumae 87803 in F nipponica 85062 inF nubicola and 99674 in F orientalis About 471 (3282Mb) of F x ananassa genome consists of repeats In case ofwild relatives 317 (633Mb) in F iinumae 255 (526Mb)in F nipponica 245 (499Mb) in F nubicola and 263(562Mb) in F orientalis are repeat regions in genome [20]
24 Prunus Prunus fruit has attractive bright shiny skincolor subtle flavor and sweetness It has long generation timeand bigger plant size It needs 3-5 years for floweringfruitproduction from planting Processed cherry product is soldworldwide
241 Chinese Plum and Japanese Apricot (Prunus mume)Prunus mume is the first plant in Prunoideae subfamilyto be sequenced Domestication of P mume could havestarted 3000 years ago in China [21] This woody perennialis considered as the first tree to be bloomed during thetransition from winter to spring at lesser than 0∘C [22]
Out of 280Mb of the genome size 2370Mb (846)was sequenced Totally 31390 protein-coding genes werecharacterized in the P mume Genome of P mume pro-vides information about the 1154 candidate genes involvedin flower aroma flowering time and disease resistanceAssembled genome contains 1068Mb (450) of repetitivesequences Investigation of P mume genome with the Vitisvinifera paleohexaploid ancestor showed that 27819 genemodels aligned with its seven ancestral chromosomes It isnoteworthy that 2772 orthologsrsquo (781) collinearity blockswere present in the P mume genome (Table 1) Comparativeanalysis of P mume chromosome with the Rosaceae ancestralchromosome showed that 4 5 and 7 chromosomes of Pmume does not undergo any changes and they are directRosaceae ancient chromosomes such as III VII and VIrespectively [23]
242 Peach (Prunus persica) Peach is one of great fruitthat provides vitamins minerals fiber and antioxidant com-pounds Peach fruit is also called nectarine due to smoothskin without fuzz or short hairs Selection and domesticationof peach could have started in Yangzi River valley Chinaaround 7500 years ago [24]
Whole genome analysis of P persica L ldquoLovellrdquo covered2246Mb (847) of genome (estimated total size 265Mb)and represented 27852 protein-coding genes Repetitivesequences present in peach were estimated as 8441Mb(3714) which is lesser than the apple (424) and grape(445) 6726Mb (2960) 2056 Mb (905) and 1714Mb(754) appeared as TEs DNA transposons and unclassifiedrepeats respectively [25] Recently P persica ldquoLovellrdquo doublehaploid genome version 20 was released with deep rese-quencing approach Assembled genome of 2274Mb (858)contains 26873 genes [26]
243 Sweet Cherry (Prunus avium) Prunus avium generallycalled sweet cherry is an important drupe fruit in the Rosaceafamily Sweet cherry is used for human consumption andwildcherry trees for wood which is also called mazzards Sweetcherry and sour cherry are the most commercial and ediblecrops in Prunus genus [27]
Genome size of P avium is about approximately 350MbShirasawa et al (2017) assembled about 778 (2724Mb) ofthe P avium ldquoSatonishikirdquo About 438 (1194Mb) of the Pavium genome were covered with the repetitive sequencesAmong the 1194Mb of repeats 851Mb of repeats are uniqueto P avium ldquoSatonishikirdquo Identified genes clustered with theP persica P mume M domestica and F vesca 75627 genesclusters are formed 3459 clusters (4535 genes) fromP aviumare present in all the investigated species and 16151 clusters(21642 genes) were found only in the P avium with theabsence of 869 clusters [28]
25 Rose Roses are one of the most essential ornamentalplants worldwide Ornamental value of rose enjoyed sincethe dawn of civilization Cultivation of roses traced back to3000 years ago It consists of 200 species and most of themare polyploid It has also been cultivated for its cosmeticvalues such as perfumes and antiques and also some of thephytochemicals of roses have high therapeutic values Rosehips can be used to cure osteoarthritis [29]
251 Rosa chinensis Rosa chinensis is one of the importantpot-type rose cultivars Recently Raymond et al (2018)sequenced the whole genome of R chinensis ldquoOld Blushrdquoand resequenced the major genotypes contributed for rosedomestication Totally 503Mb (977) of the genome wasassembled Genome results comprised 36377 protein-codinggenes 3971 long noncoding RNAs and 207 miRNAs In thegenome TEs were present about 679 From that 506were identified as long-terminal-repeat retrotransposons[30] From the doubled-haploid rose line of R chinensisldquoOld Blushrdquo (ldquoHapOBrdquo) about 901 to 961 (512Mb) ofgenomewas assembled About 466 Mbwas anchored to sevenpseudo-chromosomes and the remaining were assignedto the chromosome 0 (Chr0) Totally 44481 genes were
BioMed Research International 5
identified including 39669 protein-coding and 4812 noncod-ing genes Repeats covered about 2796Mb of genome [31]Rosa and Fragaria genomes shared the eight chromosomesof ancestral Rosaceae with one chromosome fission and twofusions Divergence of Rosa Fragaria and Rubus could haveoccurred within a short period [30] Synteny analysis showedthat chromosomes 1 4 5 6 and 7 of R chinensis havehigher collinearity with chromosomes 7 4 3 2 and 5 of Fvesca Interestingly chromosomes 2 and 3 of R chinensisweredetected as reciprocal translocation with chromosomes 6 and1 of F vesca [31]
252 Rosa multiflora Rosa multiflora is a five-petal plantbelongs to the section Synstylae It is native to the easternAsian regions [32] R multiflora was used for breedingpurpose to the modern roses Especially its resistance locus(Rdr1) tolerance against powdery mildew was introgressedwith the R hybrida [33]
Genome size of R multiflora was estimated as 750Mband about 711Mb was sequenced Assembled genome wascharacterized with 67380 genes (54893 complete genesand 12487 partial genes) Repeat regions covered 564(4172Mb) of assembled genome Out of 18956 gene clustersin R multiflora 1287 904 and 241 clusters were shared withthe F vesca P persica and M x domestica respectively Rmultiflora shared more number of gene clusters with theF vesca than the other two plants of Rosaceae Howeverunique gene clusters and genes of R multiflora are 25 (3482of R multiflora and 1397 of F vesca) and 33 (14663 of Rmultiflora and 4482 of F vesca) times higher than the F vescarespectively [34]
3 Functional Genomics
31 Fruit Development and Sucrose Metabolism in ApplePome is a unique nature of false fruit formation from thebasal part of sepals and receptacles Velasco et al (2010)suggest that pome could have evolved recently from Maleaespecific WGD which could be a major factor contributing toapple development and its specificity [11] Genes encodingfor like-hetero chromatin protein 1 (LHP1) such asMdLHP1aand MdLHP1b regulate the flowering time of apple [35]Flowering locus T1 (MdFT1) can promote flowering whereasterminal flower (MdTFL1 and MdTFL2) expressed in thevegetative part could repress flowering and maintains thevegetative meristem identity [36] Soon after fertilizationhigher expression of two cyclin-dependent kinase (CDK)bgenes and one cyclin-dependent kinase regulatory subunit(CKS) 1 indicates the active cell division of fruits [37] Tran-scription factors such asAgamous (AG) Fruitfull (FUL) AG-like (AGL)1AGL5 Spatula (SPT) Crabs Claw (CRC) andEttin (ETT) regulate the carpel identity and differentiation[38] Microarray data on apple reported that SPT ETTAuxinResponse Factor (ARF) 3 FULAGL8 and CRC transcriptswere abundant during the fruit enlargement stage Howevermost of their expressions are downregulated in cell divisionstage [39] In apple fruit development-related gene familiessuch asMADS-box genes carbohydrate metabolism sorbitolassimilation and transportation were expanded more than
the cucumber soybean poplar A thaliana grape riceBrachypodium sorghum and maize [11] Expression of 120572-expansin (120572-EXP)was detected only during the cell expansionphase of apple [39] MdMADS21 and MdMADS22 orthol-ogous to FUL-like genes in A thaliana were progressivelyinvolved in the fruit developmental process Among twocandidate genes MdMADS21 was closely associated withfruit flesh firmness [40] ARF106 gene expressed duringcell division and cell expansion stages is consistent with apotential role in the control of fruit size [41] Methylation ofDNAplays an essential role in the fruit size [12] Comparativestudy between the bigger size apple (Golden Delicious) andsmaller size apple (GDDH18) showed that twenty-two genesfound as responsible for small size have lesser methylation inthe promoter region [6]
After pollination the small amount of starch present inthe floral buds starts to metabolize Conversion of carbonto sucrose was mediated by the tonoplast monosaccharidetransporters (TMTs) MdTMT1 and MdTMT2 Expansion offruit cells is associated with the starch accumulation Higherexpression of sorbitol dehydrogenase (SHD) cell wall invertase(CIN) neutral invertase (NIN) sucrose synthase (SS) fruc-tokinase (FRK) and hexokinase (HK) indicates the metabo-lization of sorbitol and sucrose [42] In the early period ofcell expansion starch accumulation was higher and it startsto decline in the later phase [11] Transcript of SS genes inapple is correlated with the starch accumulation [39] Sorbitoldehydrogenase (SDH) converts carbohydrate into fructoseNine SDH genes were identified in apple fruit [43] In youngfruit MdSDH1 expression was higher than in mature fruit[42] Other genes significantly upregulated during ripeningstage are isopentenyl pyrophosphate (IPP) isomerase catalase(CAT) histone 2B (H2B) and the ripening-inhibitor (RIN)MADS-box gene [39] During the ripening process a decreaseof starch synthesis is vice versa with the sugar level [44]Expression profiles of sucrose-phosphatase phosphatase (SPP)and sucrose-phosphate synthase (SPS) were active in the ripen-ing stage [42] suggesting that these enzymesmay be involvedin starch degradation pathway Polygalacturonase 1 (MdPG1)and aminocyclopropane-1-carboxylate oxidase (MdACO1)were involved in the fruit softening and ethylene biosynthesisin apple respectively [45] Decrease in the expression ofPG1 alters the firmness tensile strength and water loss inapple M x domestica fruit [46] MeanwhileMdFT1MdACS1(1-aminocyclopropane-1-carboxylic acid synthase) MdACO1and MdExp7 are regulating the fruit softening Amongthem MdExp7 and MdACO1 control firmness in apple [45]Gene coding for MYB TF in apple MdMyb1 increases theanthocyanin content and is responsible for the red skin color[47] Acidity in apple is due to the malic acid and mamarecessive gene is responsible for low acidity [48]
In apple fruit size sugar content and palatability areessential qualities determining its marketability Knowledgeof genes governing the fruit quality could be essential forscreening better linesgenotypes for breeding
32 Lignin Metabolism and Stone Cell Formation in PearStone cell content is the main quality determinant of pearfruit Deposition of lignin on the primary cell wall of
6 BioMed Research International
Lignin synthesis
Branchy sclereids
Stone cells
HCT
LIMMYB
PbCAD2
PbCCR2
PbCCR1
PbCCR3
CCOMTC3H
NAC (NAM ATAF12 and CUC2)
Figure 1 Simple heuristic representation of genestranscription factors involved in lignin synthesis and stone cell formation in pearfruit Pb Pyrus bretschneideri hydroxycinnamoyl transferase HCT p-coumaroyl-shikimatequinate 31015840-hydroxylases C31015840H caffeoyl-CoA O-methyltransferase CCOMT NAM ATAF12 and CUC2 NAC Lin11Isl1Mec3 LIM myeloblastosis MYB cinnamyl alcohol dehydrogenaseCAD and cinnamoyl-CoA reductase CCR Red colored dots represent the stone cells
parenchyma cell followed by the secondary sedimentation ona sclerenchyma cell forms the stone cells Majority of stonecells present in pear is branchy sclereids comprised lignin andcellulose Lignins are synthesized by twoways one starts withp-coumaric acid and second with phenylalanine precursorto cinnamic acid and then p-coumaric acid Other forms oflignin monomers are caffeic acid ferulic acid 5-hydroxy-ferulic acid and sinapinic acid [49ndash51] Finallymonomers arepolymerized to form lignin products Monomers of lignin arecategorized into three types syringly lignin (S-lignin) guaia-cyl lignin (G-lignin) and hydroxyphenyl lignin (H-lignin)From the gnome analysis a total of 66 lignin synthesis-related gene families were characterized in P bretschneideriIt signifies the high demand for lignin synthesis in pear [15]In ldquoDangshan Surdquo pulp milled wood lignin was identifiedas guaiacyl-syringyl-lignin It was observed that ldquoDangshanSurdquo lignin possesses more guaiacyl units than the syringylunits [49] Hydroxycinnamoyl transferases (HCT) play asignificant role in the lignin synthesis [52] Accumulation ofG-lignin and S-lignin is interrelated with theHCT expressionespecially at early fruit developmental stage [15]
Cinnamoyl-CoA reductase (CCR) and cinnamyl alco-hol dehydrogenase (CAD) belonging to medium-or-short-chain dehydrogenasereductase are key enzymes for ligninmonomer synthesis [53] Totally 31 CCRs and 26 CADsgenes were identified in P bretschneideri ldquoDangshan Surdquo Allmembers of CCR and CAD identified in P bretschneideri arenot involved in the lignin biosynthesis [54] Among them
PbCAD2 PbCCR1 PbCCR2 and PbCCR3 were identified toparticipate in the lignin synthesis of stone cells [15] NAC(NAM ATAF12 and CUC2) and LIM (Lin11Isl1Mec3) arean important TF influencing the lignin pathway [55 56]Mostof theCCR andCADmembers present in the pear possess SPL(squamosal promoter binding-like) light-responsive elementon their upstream Functions of PbCCR and PbCAD arerelated to the light signaling Presence of MYB-binding ACcis elements in some promoter of the PbCCRs suggestedthat phenylpropanoid metabolism of lignin synthesis wasregulated by MYB transcription factors Similarly TGACG-motif on some PbCCRs and all PbCADrsquos promoter regionsrevealed their involvement in the abscisic acid jasmonicacid andmethyl jasmonic acidmetabolism [15]The pictorialillustration of genesTFs required for the lignin synthesis aswell as stone cell formation is mentioned in Figure 1
There are many internal and external factors involved inthe stone cell formation of pear Identification of candidategenes of lignin biosynthesis and stone cell formation willbe very much useful to improve the cultural practices forproducing pear fruits with different palatable level of stonecells
33 Fruit Aroma and Softness in Strawberry Strawberry iswidely appreciated for its delicate flavor aroma and nutri-tional value Aroma of strawberry is due to esters alcoholsaldehydes and sulfur compounds Hundreds of volatile estershave been correlated with strawberry ripening and aroma
BioMed Research International 7
[57] Volatile esters are the major constituents of floral scentWild species such as F vesca and F virginiana have muchstronger aroma than the cultivated types Compared to theregular octoploid strawberry unique phenolic compoundswere found inF vesca fruits such as taxifolin 3-O-arabinosideand peonidin 3-O-malonylglucoside [58] Pinene synthase(PINS) is primarily expressed in wild strawberry whileinsertional mutation reduced its expression in cultivatedspecies F vesca contains high amounts of ethyl-acetate andlower methyl-butyrate ethyl-butyrate and furanone levels Fnilgerrensis possesses higher ethyl-acetate and furanone butlower methyl-butyrate and ethyl-butyrate Hybrids betweenF vesca and F ananassa have intermediate contents of fra-grance and aroma related compounds while crosses betweenF nilgerrensis and F ananassa more closely resemble Fnilgerrensis [17] Volatile compounds found to be responsiblefor general strawberry smell are 2 5-dimethyl-4-hydroxy-3(2H)-furanone linalool and ethyl hexanoate Neverthelessethyl butanoate methyl butanoate 120574-decalactone and 2-heptanone are represented as cultivar specific aroma com-pounds [59] O-methyltransferase of strawberry (FaOMT) isvital for the biosynthesis of vanillin and furaneol [60]Alcoholacyltransferase (AATs) in strawberry (SAAT) is involved inthe last step of volatile esters synthesis and vital for flavorbiogenesis in ripening fruit SAAT catalyzes esterificationof an acyl moiety from actyl-CoA to alcohol [61] Straw-berry quinone oxidoreductase (FaQR) is required for thebiosynthesis of furaneol Furaneol and its methoxy derivative(methoxyfuraneol and mesifuran) are catalyzed by OMT Allthree furaneol compounds are highly accumulated duringfruit ripening stage [62] Though two types of pyruvatedecarboxylase (PDC) were identified in strawberry onlyFaPDC1 was induced during fruit ripening [63]
Strawberry is highly perishable even with controlledatmospheric storage Higher proportion of fruit last occurreddue to its softness and sensitivity to fungal disease Redcolored strawberry showed the higher level of anthocyanin-related transcripts [64] FcMYB1 could regulate branching-point of the anthocyaninproanthocyanidin biosynthesisFaWRKY1 mediate defense response and FaPE1 encodedfor pectin methyl esterase are conferred at least with apartial resistance of ripened fruit against Botrytis cinerea[65 66] Polygalacturonase 1 of F x ananassa (FaPG1) iscritical for fruit softening [67] In strawberry fruits beta-D-glucosyltransferase (FaGT) correlated with the relevantphenylpropanoid glucosides [68]D-xylose reductase (FaXyl1)and beta-xylosidase activity were higher in ldquoToyonakardquo (soft)than in the ldquoCamarosardquo (firm) showing the correlationbetween FaXyl1 expression and fruit softening [69] Fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase) is involvedin the firmness and postharvest life [70] A lesser activity ofbeta-galactosidase (120573Gal) and 120573Xyl activity were correlatedwith decreased fruit firmness in F chiloensis and F timesananassa respectively [71] Expression of FaCCR is higherin soft fruit cultivar (Gorella) whereas FaCAD is higher infirm fruit cultivar (Holiday) [72] Expression of five expansingenes (FaEXP1 FaEXP2 FaEXP4 FaEXP5 and FaEXP6) wasstudied in cultivars with different firmness ldquoSelvardquo (hard)ldquoCamarosardquo (medium) and ldquoToyonakardquo (soft) Higher level
of FaEXP1 FaEXP2 and FaEXP5 expression was foundin fruit with less firmness (ldquoToyonakardquo) than the othertwo cultivars (ldquoSelvardquo and ldquoCamarosardquo) Fruit firmnessis identified to be associated with pectate lyase (FaPel1)identified Expansin activity was characterized by cell wallmodification [73] Polysaccharides were modified by fivedifferent genes such as FasPG FaPG-like FaPel1 FaPel2 andFaEXP2 [74] Sorbitol dehydrogenase (FaSDH) and sorbitol-6-phosphate dehydrogenase (FaS6PDH) genes are involved withthe sorbitol synthesis in leaves fruits and shoot tips [75]SEPALLATA (SEP)4-like gene FaMADS9 is responsible forthe fruit ripening [76]
Apart from the aesthetic and taste mechanisms of flower-ing and its response to the light signaling in strawberry needto be studied in detail Cultivars with continuous floweringand growing underminimal light energy are beneficial for thestrawberry growers as most of the commercial cultivation iscarried out in the controlled greenhouse
34 Early Blooming and Fruit Ripening in Prunus Prunusis the first plant to bloom in later winterearly spring Soit is the best model plant to study early flowering as wellas chilling tolerance Dehydrins are known as 2 or D-11family late-embryogenesis-abundant (LEA) proteins Theyplay a vital role in plant growth and cold tolerance [77] InP mume 30 LEA genes were characterized and classifiedinto eight groups LEA1 LEA2 LEA3 LEA4 LEA5 PvLEA18dehydrin and seed maturation protein Out of 30 identifiedgenes 22 were expressed in flowers and 19 were inducedby abscisic acid (ABA) treatments [78] Molecular cloningof PmLEA8 PmLEA10 PmLEA19 PmLEA20 and PmLEA29showed that except PmLEA8 all other genes enhancedthe freezing-tolerance Interestingly among all cold-resistantLEA genemembers studied only PmLEA19were upregulatedfour timeswhen the branches of Pmumewere exposed to 4∘C[79]Downregulation inPmume dormancy associatedMADS(PmDAM) 4 PmDAM5 and PmDAM6 expression releasesthe endodormancy [80] Among the six DAM genes exceptPmDAM3 all other genes are responsive to the photoperiodand seasonal (cold) responses [81] In P persica from six iden-tified DAM genes PpDAM5 and PpDAM6 were character-ized to be involved in the lateral bud dormancy breakage [82]DAM5 and DAM6 were identified as homologous to ShortVegetative Phase (SVP)AGL 24 in A thaliana Both SVPand AGL-24 are required for floral meristem identity [83]AGL24 is well known for promoting early flowering and floraltransition in plants [58] Transcriptome analysis betweencold sensitive (ldquoMorettinirdquo) and cold tolerant (ldquoRoyal Gloryrdquo)cultivars in P persica showed that 120573-D-xylosidase (BXL)and pathogen-related protein 4b (PR-4B) were significantlyexpressed only in resistant variety [84] Other candidategenes identified as required to control flowering time aresuppressor of phyA (SPA) COP1 interacting protein8 (CIP8)phytochrome A (phyA) and phytochrome interacting factor 3(PIF3) [85] Figure 2 demonstrates the important key genesinvolved in cold tolerance early blooming and floweringtime control of P mume Higher number of aesthetic prop-erties related genes such as benzyl alcohol acetyltransferase(BEAT) (34) are identified in P mume Only 16 in Malus x
8 BioMed Research International
PmLEA19 PmDAM4 PmDAM5 and PmDAM6
SPA CIP8 phyA and PIF3BXL and PR-4B
Cold toler
ance
Cold tolerance
Control flowering time
Dorman
cy re
lease
Figure 2 Factors involved in the early blooming of Chinese plumJapanese apricot Prunus meme Pm late-embryogenesis-abundant LEAdormancy associated MADS DAM 120573-D-xylosidase BXL pathogen-related protein 4b PR-4B suppressor of phyA SPA COP1 interactingprotein8 CIP8 phytochrome A phyA and phytochrome interacting factor3 PIF3 The lower arrow represents downregulation
domestica 14 in F vesca 4 inVitis vinifera 17 in P trichocarpaand 3 inA thaliana of BEAT genes were identifiedThereforein P mume BEAT genes are considered as key factor todetermine its exclusive floral fragrance [23]
In Prunus UDP-glucose-flavonoid-3-O-glucosyltransfer-ase (UFGT) expression was higher during the initial periodand it is reduced on the developmental process Duringthe ripening processMYB10 MYB123 and basic-helix-loop-helix (bHLH3)were upregulatedwhereasMYB16 andMYB111were downregulated Higher anthocyanin and Proantho-cyanidin levels were correlatedwith theMYB10 andMYBPA1respectively Stimulation of TFs is responsive for the devel-opment and external stimuli [86] Gene encoding ethylene-responsive transcription factor (ERF)4 is necessary for the fruitmaturity [87] Though 74 EFR genes were predicted in thepeach genome only one copy of ERF4 has existed ThereforeERF4 is vital to control the fruit maturity and ripening inpeach [85] An initial stage of fruit has higher aldehyde andalcohol production whereas later stages have lesser contentwhich is correlated with the ester production Abundance ofalcohol dehydrogenase (ADH) and lipoxygenase (LOX) geneis constant in the fruit development stages Expression ofAATwas sharply increased in the later stage of harvest [88] Rapidsoftening of fruits was related to the ethylene productionin P persica It is correlated with expression of PpACS1 (1-aminocyclopropane-1-carboxylic acid synthase) [89] Ripenedsweet cherry P avium has unique fragrance In the sweetcherry (ldquoHongdengrdquo ldquoHongyanrdquo and ldquoRainierrdquo) 97 volatilecompounds were identified Alcohols and terpenes were thepredominant components of bound volatiles Benzyl alcoholgeraniol and 2-phenylethanol are the major bound volatileconstituents Free volatile compounds majorly present insweet cherry are hexanal 2-hexenal 2-hexen-1-ol benzyl
alcohol and benzaldehyde Free volatiles are responsible forfloral aroma and bound volatiles involved in fruit freshnessDepending on the level of free and bound volatiles aroma andglycosidically bound compounds aroma and fruit firmnesswere varied between the cultivars of sweet cherry [90]
In Prunus apricot peach sweet cherry and sour cherryare widely used for human consumption Comparativegenomics study between the species offer the candidate geneto produce hybrids with more preferable qualities
35 Blooming and Scent Pathways in Rose Continuous flow-ering (CF)recurrent blooming (RB) genotypes flowers in allfavorable seasons whereas once-flowering (OF) genotypesonly flowers in spring Recurrent blooming is an importanttrait required by breeders R x hybrida ldquoLa Francerdquo was thefirst hybrid combined with the growth vigor of Europeanspecies and recurrent blooming of Chinese species It hasthe complex genetic pool combination of three ancestralgenotypes such as Cinnamomeae Synstylae and ChinensesInsertion of TE in the TFL1 encodes gene Ksncopia (KSN)was found as responsible for the recurrent blooming of ldquoLaFrancerdquo [30] Previously Horibe et al (2013) reported thatKSN gene regulates the CF behavior of R rugosa [91] Wanget al (2012) studied recurrent flowering character and theexpression patterns of TFL1 homologs in R multiflora Rrugosa R chinensis and other speciescultivars Among thethree orthologs RTFL1c was highly expressed at all fourflowering stages in R multiflora and R rugosa (nonrecurrentflowering species) and barely detected in R chinensis (arecurrent flowering species) at any stage Therefore it can beconsidered that lower expression of RTFL1c is required forrecurrent flowering of roses [92] Iwata et al (2012) elucidatethat occurrence of TE insertion and point mutation in the
BioMed Research International 9
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
identified including 39669 protein-coding and 4812 noncod-ing genes Repeats covered about 2796Mb of genome [31]Rosa and Fragaria genomes shared the eight chromosomesof ancestral Rosaceae with one chromosome fission and twofusions Divergence of Rosa Fragaria and Rubus could haveoccurred within a short period [30] Synteny analysis showedthat chromosomes 1 4 5 6 and 7 of R chinensis havehigher collinearity with chromosomes 7 4 3 2 and 5 of Fvesca Interestingly chromosomes 2 and 3 of R chinensisweredetected as reciprocal translocation with chromosomes 6 and1 of F vesca [31]
252 Rosa multiflora Rosa multiflora is a five-petal plantbelongs to the section Synstylae It is native to the easternAsian regions [32] R multiflora was used for breedingpurpose to the modern roses Especially its resistance locus(Rdr1) tolerance against powdery mildew was introgressedwith the R hybrida [33]
Genome size of R multiflora was estimated as 750Mband about 711Mb was sequenced Assembled genome wascharacterized with 67380 genes (54893 complete genesand 12487 partial genes) Repeat regions covered 564(4172Mb) of assembled genome Out of 18956 gene clustersin R multiflora 1287 904 and 241 clusters were shared withthe F vesca P persica and M x domestica respectively Rmultiflora shared more number of gene clusters with theF vesca than the other two plants of Rosaceae Howeverunique gene clusters and genes of R multiflora are 25 (3482of R multiflora and 1397 of F vesca) and 33 (14663 of Rmultiflora and 4482 of F vesca) times higher than the F vescarespectively [34]
3 Functional Genomics
31 Fruit Development and Sucrose Metabolism in ApplePome is a unique nature of false fruit formation from thebasal part of sepals and receptacles Velasco et al (2010)suggest that pome could have evolved recently from Maleaespecific WGD which could be a major factor contributing toapple development and its specificity [11] Genes encodingfor like-hetero chromatin protein 1 (LHP1) such asMdLHP1aand MdLHP1b regulate the flowering time of apple [35]Flowering locus T1 (MdFT1) can promote flowering whereasterminal flower (MdTFL1 and MdTFL2) expressed in thevegetative part could repress flowering and maintains thevegetative meristem identity [36] Soon after fertilizationhigher expression of two cyclin-dependent kinase (CDK)bgenes and one cyclin-dependent kinase regulatory subunit(CKS) 1 indicates the active cell division of fruits [37] Tran-scription factors such asAgamous (AG) Fruitfull (FUL) AG-like (AGL)1AGL5 Spatula (SPT) Crabs Claw (CRC) andEttin (ETT) regulate the carpel identity and differentiation[38] Microarray data on apple reported that SPT ETTAuxinResponse Factor (ARF) 3 FULAGL8 and CRC transcriptswere abundant during the fruit enlargement stage Howevermost of their expressions are downregulated in cell divisionstage [39] In apple fruit development-related gene familiessuch asMADS-box genes carbohydrate metabolism sorbitolassimilation and transportation were expanded more than
the cucumber soybean poplar A thaliana grape riceBrachypodium sorghum and maize [11] Expression of 120572-expansin (120572-EXP)was detected only during the cell expansionphase of apple [39] MdMADS21 and MdMADS22 orthol-ogous to FUL-like genes in A thaliana were progressivelyinvolved in the fruit developmental process Among twocandidate genes MdMADS21 was closely associated withfruit flesh firmness [40] ARF106 gene expressed duringcell division and cell expansion stages is consistent with apotential role in the control of fruit size [41] Methylation ofDNAplays an essential role in the fruit size [12] Comparativestudy between the bigger size apple (Golden Delicious) andsmaller size apple (GDDH18) showed that twenty-two genesfound as responsible for small size have lesser methylation inthe promoter region [6]
After pollination the small amount of starch present inthe floral buds starts to metabolize Conversion of carbonto sucrose was mediated by the tonoplast monosaccharidetransporters (TMTs) MdTMT1 and MdTMT2 Expansion offruit cells is associated with the starch accumulation Higherexpression of sorbitol dehydrogenase (SHD) cell wall invertase(CIN) neutral invertase (NIN) sucrose synthase (SS) fruc-tokinase (FRK) and hexokinase (HK) indicates the metabo-lization of sorbitol and sucrose [42] In the early period ofcell expansion starch accumulation was higher and it startsto decline in the later phase [11] Transcript of SS genes inapple is correlated with the starch accumulation [39] Sorbitoldehydrogenase (SDH) converts carbohydrate into fructoseNine SDH genes were identified in apple fruit [43] In youngfruit MdSDH1 expression was higher than in mature fruit[42] Other genes significantly upregulated during ripeningstage are isopentenyl pyrophosphate (IPP) isomerase catalase(CAT) histone 2B (H2B) and the ripening-inhibitor (RIN)MADS-box gene [39] During the ripening process a decreaseof starch synthesis is vice versa with the sugar level [44]Expression profiles of sucrose-phosphatase phosphatase (SPP)and sucrose-phosphate synthase (SPS) were active in the ripen-ing stage [42] suggesting that these enzymesmay be involvedin starch degradation pathway Polygalacturonase 1 (MdPG1)and aminocyclopropane-1-carboxylate oxidase (MdACO1)were involved in the fruit softening and ethylene biosynthesisin apple respectively [45] Decrease in the expression ofPG1 alters the firmness tensile strength and water loss inapple M x domestica fruit [46] MeanwhileMdFT1MdACS1(1-aminocyclopropane-1-carboxylic acid synthase) MdACO1and MdExp7 are regulating the fruit softening Amongthem MdExp7 and MdACO1 control firmness in apple [45]Gene coding for MYB TF in apple MdMyb1 increases theanthocyanin content and is responsible for the red skin color[47] Acidity in apple is due to the malic acid and mamarecessive gene is responsible for low acidity [48]
In apple fruit size sugar content and palatability areessential qualities determining its marketability Knowledgeof genes governing the fruit quality could be essential forscreening better linesgenotypes for breeding
32 Lignin Metabolism and Stone Cell Formation in PearStone cell content is the main quality determinant of pearfruit Deposition of lignin on the primary cell wall of
6 BioMed Research International
Lignin synthesis
Branchy sclereids
Stone cells
HCT
LIMMYB
PbCAD2
PbCCR2
PbCCR1
PbCCR3
CCOMTC3H
NAC (NAM ATAF12 and CUC2)
Figure 1 Simple heuristic representation of genestranscription factors involved in lignin synthesis and stone cell formation in pearfruit Pb Pyrus bretschneideri hydroxycinnamoyl transferase HCT p-coumaroyl-shikimatequinate 31015840-hydroxylases C31015840H caffeoyl-CoA O-methyltransferase CCOMT NAM ATAF12 and CUC2 NAC Lin11Isl1Mec3 LIM myeloblastosis MYB cinnamyl alcohol dehydrogenaseCAD and cinnamoyl-CoA reductase CCR Red colored dots represent the stone cells
parenchyma cell followed by the secondary sedimentation ona sclerenchyma cell forms the stone cells Majority of stonecells present in pear is branchy sclereids comprised lignin andcellulose Lignins are synthesized by twoways one starts withp-coumaric acid and second with phenylalanine precursorto cinnamic acid and then p-coumaric acid Other forms oflignin monomers are caffeic acid ferulic acid 5-hydroxy-ferulic acid and sinapinic acid [49ndash51] Finallymonomers arepolymerized to form lignin products Monomers of lignin arecategorized into three types syringly lignin (S-lignin) guaia-cyl lignin (G-lignin) and hydroxyphenyl lignin (H-lignin)From the gnome analysis a total of 66 lignin synthesis-related gene families were characterized in P bretschneideriIt signifies the high demand for lignin synthesis in pear [15]In ldquoDangshan Surdquo pulp milled wood lignin was identifiedas guaiacyl-syringyl-lignin It was observed that ldquoDangshanSurdquo lignin possesses more guaiacyl units than the syringylunits [49] Hydroxycinnamoyl transferases (HCT) play asignificant role in the lignin synthesis [52] Accumulation ofG-lignin and S-lignin is interrelated with theHCT expressionespecially at early fruit developmental stage [15]
Cinnamoyl-CoA reductase (CCR) and cinnamyl alco-hol dehydrogenase (CAD) belonging to medium-or-short-chain dehydrogenasereductase are key enzymes for ligninmonomer synthesis [53] Totally 31 CCRs and 26 CADsgenes were identified in P bretschneideri ldquoDangshan Surdquo Allmembers of CCR and CAD identified in P bretschneideri arenot involved in the lignin biosynthesis [54] Among them
PbCAD2 PbCCR1 PbCCR2 and PbCCR3 were identified toparticipate in the lignin synthesis of stone cells [15] NAC(NAM ATAF12 and CUC2) and LIM (Lin11Isl1Mec3) arean important TF influencing the lignin pathway [55 56]Mostof theCCR andCADmembers present in the pear possess SPL(squamosal promoter binding-like) light-responsive elementon their upstream Functions of PbCCR and PbCAD arerelated to the light signaling Presence of MYB-binding ACcis elements in some promoter of the PbCCRs suggestedthat phenylpropanoid metabolism of lignin synthesis wasregulated by MYB transcription factors Similarly TGACG-motif on some PbCCRs and all PbCADrsquos promoter regionsrevealed their involvement in the abscisic acid jasmonicacid andmethyl jasmonic acidmetabolism [15]The pictorialillustration of genesTFs required for the lignin synthesis aswell as stone cell formation is mentioned in Figure 1
There are many internal and external factors involved inthe stone cell formation of pear Identification of candidategenes of lignin biosynthesis and stone cell formation willbe very much useful to improve the cultural practices forproducing pear fruits with different palatable level of stonecells
33 Fruit Aroma and Softness in Strawberry Strawberry iswidely appreciated for its delicate flavor aroma and nutri-tional value Aroma of strawberry is due to esters alcoholsaldehydes and sulfur compounds Hundreds of volatile estershave been correlated with strawberry ripening and aroma
BioMed Research International 7
[57] Volatile esters are the major constituents of floral scentWild species such as F vesca and F virginiana have muchstronger aroma than the cultivated types Compared to theregular octoploid strawberry unique phenolic compoundswere found inF vesca fruits such as taxifolin 3-O-arabinosideand peonidin 3-O-malonylglucoside [58] Pinene synthase(PINS) is primarily expressed in wild strawberry whileinsertional mutation reduced its expression in cultivatedspecies F vesca contains high amounts of ethyl-acetate andlower methyl-butyrate ethyl-butyrate and furanone levels Fnilgerrensis possesses higher ethyl-acetate and furanone butlower methyl-butyrate and ethyl-butyrate Hybrids betweenF vesca and F ananassa have intermediate contents of fra-grance and aroma related compounds while crosses betweenF nilgerrensis and F ananassa more closely resemble Fnilgerrensis [17] Volatile compounds found to be responsiblefor general strawberry smell are 2 5-dimethyl-4-hydroxy-3(2H)-furanone linalool and ethyl hexanoate Neverthelessethyl butanoate methyl butanoate 120574-decalactone and 2-heptanone are represented as cultivar specific aroma com-pounds [59] O-methyltransferase of strawberry (FaOMT) isvital for the biosynthesis of vanillin and furaneol [60]Alcoholacyltransferase (AATs) in strawberry (SAAT) is involved inthe last step of volatile esters synthesis and vital for flavorbiogenesis in ripening fruit SAAT catalyzes esterificationof an acyl moiety from actyl-CoA to alcohol [61] Straw-berry quinone oxidoreductase (FaQR) is required for thebiosynthesis of furaneol Furaneol and its methoxy derivative(methoxyfuraneol and mesifuran) are catalyzed by OMT Allthree furaneol compounds are highly accumulated duringfruit ripening stage [62] Though two types of pyruvatedecarboxylase (PDC) were identified in strawberry onlyFaPDC1 was induced during fruit ripening [63]
Strawberry is highly perishable even with controlledatmospheric storage Higher proportion of fruit last occurreddue to its softness and sensitivity to fungal disease Redcolored strawberry showed the higher level of anthocyanin-related transcripts [64] FcMYB1 could regulate branching-point of the anthocyaninproanthocyanidin biosynthesisFaWRKY1 mediate defense response and FaPE1 encodedfor pectin methyl esterase are conferred at least with apartial resistance of ripened fruit against Botrytis cinerea[65 66] Polygalacturonase 1 of F x ananassa (FaPG1) iscritical for fruit softening [67] In strawberry fruits beta-D-glucosyltransferase (FaGT) correlated with the relevantphenylpropanoid glucosides [68]D-xylose reductase (FaXyl1)and beta-xylosidase activity were higher in ldquoToyonakardquo (soft)than in the ldquoCamarosardquo (firm) showing the correlationbetween FaXyl1 expression and fruit softening [69] Fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase) is involvedin the firmness and postharvest life [70] A lesser activity ofbeta-galactosidase (120573Gal) and 120573Xyl activity were correlatedwith decreased fruit firmness in F chiloensis and F timesananassa respectively [71] Expression of FaCCR is higherin soft fruit cultivar (Gorella) whereas FaCAD is higher infirm fruit cultivar (Holiday) [72] Expression of five expansingenes (FaEXP1 FaEXP2 FaEXP4 FaEXP5 and FaEXP6) wasstudied in cultivars with different firmness ldquoSelvardquo (hard)ldquoCamarosardquo (medium) and ldquoToyonakardquo (soft) Higher level
of FaEXP1 FaEXP2 and FaEXP5 expression was foundin fruit with less firmness (ldquoToyonakardquo) than the othertwo cultivars (ldquoSelvardquo and ldquoCamarosardquo) Fruit firmnessis identified to be associated with pectate lyase (FaPel1)identified Expansin activity was characterized by cell wallmodification [73] Polysaccharides were modified by fivedifferent genes such as FasPG FaPG-like FaPel1 FaPel2 andFaEXP2 [74] Sorbitol dehydrogenase (FaSDH) and sorbitol-6-phosphate dehydrogenase (FaS6PDH) genes are involved withthe sorbitol synthesis in leaves fruits and shoot tips [75]SEPALLATA (SEP)4-like gene FaMADS9 is responsible forthe fruit ripening [76]
Apart from the aesthetic and taste mechanisms of flower-ing and its response to the light signaling in strawberry needto be studied in detail Cultivars with continuous floweringand growing underminimal light energy are beneficial for thestrawberry growers as most of the commercial cultivation iscarried out in the controlled greenhouse
34 Early Blooming and Fruit Ripening in Prunus Prunusis the first plant to bloom in later winterearly spring Soit is the best model plant to study early flowering as wellas chilling tolerance Dehydrins are known as 2 or D-11family late-embryogenesis-abundant (LEA) proteins Theyplay a vital role in plant growth and cold tolerance [77] InP mume 30 LEA genes were characterized and classifiedinto eight groups LEA1 LEA2 LEA3 LEA4 LEA5 PvLEA18dehydrin and seed maturation protein Out of 30 identifiedgenes 22 were expressed in flowers and 19 were inducedby abscisic acid (ABA) treatments [78] Molecular cloningof PmLEA8 PmLEA10 PmLEA19 PmLEA20 and PmLEA29showed that except PmLEA8 all other genes enhancedthe freezing-tolerance Interestingly among all cold-resistantLEA genemembers studied only PmLEA19were upregulatedfour timeswhen the branches of Pmumewere exposed to 4∘C[79]Downregulation inPmume dormancy associatedMADS(PmDAM) 4 PmDAM5 and PmDAM6 expression releasesthe endodormancy [80] Among the six DAM genes exceptPmDAM3 all other genes are responsive to the photoperiodand seasonal (cold) responses [81] In P persica from six iden-tified DAM genes PpDAM5 and PpDAM6 were character-ized to be involved in the lateral bud dormancy breakage [82]DAM5 and DAM6 were identified as homologous to ShortVegetative Phase (SVP)AGL 24 in A thaliana Both SVPand AGL-24 are required for floral meristem identity [83]AGL24 is well known for promoting early flowering and floraltransition in plants [58] Transcriptome analysis betweencold sensitive (ldquoMorettinirdquo) and cold tolerant (ldquoRoyal Gloryrdquo)cultivars in P persica showed that 120573-D-xylosidase (BXL)and pathogen-related protein 4b (PR-4B) were significantlyexpressed only in resistant variety [84] Other candidategenes identified as required to control flowering time aresuppressor of phyA (SPA) COP1 interacting protein8 (CIP8)phytochrome A (phyA) and phytochrome interacting factor 3(PIF3) [85] Figure 2 demonstrates the important key genesinvolved in cold tolerance early blooming and floweringtime control of P mume Higher number of aesthetic prop-erties related genes such as benzyl alcohol acetyltransferase(BEAT) (34) are identified in P mume Only 16 in Malus x
8 BioMed Research International
PmLEA19 PmDAM4 PmDAM5 and PmDAM6
SPA CIP8 phyA and PIF3BXL and PR-4B
Cold toler
ance
Cold tolerance
Control flowering time
Dorman
cy re
lease
Figure 2 Factors involved in the early blooming of Chinese plumJapanese apricot Prunus meme Pm late-embryogenesis-abundant LEAdormancy associated MADS DAM 120573-D-xylosidase BXL pathogen-related protein 4b PR-4B suppressor of phyA SPA COP1 interactingprotein8 CIP8 phytochrome A phyA and phytochrome interacting factor3 PIF3 The lower arrow represents downregulation
domestica 14 in F vesca 4 inVitis vinifera 17 in P trichocarpaand 3 inA thaliana of BEAT genes were identifiedThereforein P mume BEAT genes are considered as key factor todetermine its exclusive floral fragrance [23]
In Prunus UDP-glucose-flavonoid-3-O-glucosyltransfer-ase (UFGT) expression was higher during the initial periodand it is reduced on the developmental process Duringthe ripening processMYB10 MYB123 and basic-helix-loop-helix (bHLH3)were upregulatedwhereasMYB16 andMYB111were downregulated Higher anthocyanin and Proantho-cyanidin levels were correlatedwith theMYB10 andMYBPA1respectively Stimulation of TFs is responsive for the devel-opment and external stimuli [86] Gene encoding ethylene-responsive transcription factor (ERF)4 is necessary for the fruitmaturity [87] Though 74 EFR genes were predicted in thepeach genome only one copy of ERF4 has existed ThereforeERF4 is vital to control the fruit maturity and ripening inpeach [85] An initial stage of fruit has higher aldehyde andalcohol production whereas later stages have lesser contentwhich is correlated with the ester production Abundance ofalcohol dehydrogenase (ADH) and lipoxygenase (LOX) geneis constant in the fruit development stages Expression ofAATwas sharply increased in the later stage of harvest [88] Rapidsoftening of fruits was related to the ethylene productionin P persica It is correlated with expression of PpACS1 (1-aminocyclopropane-1-carboxylic acid synthase) [89] Ripenedsweet cherry P avium has unique fragrance In the sweetcherry (ldquoHongdengrdquo ldquoHongyanrdquo and ldquoRainierrdquo) 97 volatilecompounds were identified Alcohols and terpenes were thepredominant components of bound volatiles Benzyl alcoholgeraniol and 2-phenylethanol are the major bound volatileconstituents Free volatile compounds majorly present insweet cherry are hexanal 2-hexenal 2-hexen-1-ol benzyl
alcohol and benzaldehyde Free volatiles are responsible forfloral aroma and bound volatiles involved in fruit freshnessDepending on the level of free and bound volatiles aroma andglycosidically bound compounds aroma and fruit firmnesswere varied between the cultivars of sweet cherry [90]
In Prunus apricot peach sweet cherry and sour cherryare widely used for human consumption Comparativegenomics study between the species offer the candidate geneto produce hybrids with more preferable qualities
35 Blooming and Scent Pathways in Rose Continuous flow-ering (CF)recurrent blooming (RB) genotypes flowers in allfavorable seasons whereas once-flowering (OF) genotypesonly flowers in spring Recurrent blooming is an importanttrait required by breeders R x hybrida ldquoLa Francerdquo was thefirst hybrid combined with the growth vigor of Europeanspecies and recurrent blooming of Chinese species It hasthe complex genetic pool combination of three ancestralgenotypes such as Cinnamomeae Synstylae and ChinensesInsertion of TE in the TFL1 encodes gene Ksncopia (KSN)was found as responsible for the recurrent blooming of ldquoLaFrancerdquo [30] Previously Horibe et al (2013) reported thatKSN gene regulates the CF behavior of R rugosa [91] Wanget al (2012) studied recurrent flowering character and theexpression patterns of TFL1 homologs in R multiflora Rrugosa R chinensis and other speciescultivars Among thethree orthologs RTFL1c was highly expressed at all fourflowering stages in R multiflora and R rugosa (nonrecurrentflowering species) and barely detected in R chinensis (arecurrent flowering species) at any stage Therefore it can beconsidered that lower expression of RTFL1c is required forrecurrent flowering of roses [92] Iwata et al (2012) elucidatethat occurrence of TE insertion and point mutation in the
BioMed Research International 9
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
Figure 1 Simple heuristic representation of genestranscription factors involved in lignin synthesis and stone cell formation in pearfruit Pb Pyrus bretschneideri hydroxycinnamoyl transferase HCT p-coumaroyl-shikimatequinate 31015840-hydroxylases C31015840H caffeoyl-CoA O-methyltransferase CCOMT NAM ATAF12 and CUC2 NAC Lin11Isl1Mec3 LIM myeloblastosis MYB cinnamyl alcohol dehydrogenaseCAD and cinnamoyl-CoA reductase CCR Red colored dots represent the stone cells
parenchyma cell followed by the secondary sedimentation ona sclerenchyma cell forms the stone cells Majority of stonecells present in pear is branchy sclereids comprised lignin andcellulose Lignins are synthesized by twoways one starts withp-coumaric acid and second with phenylalanine precursorto cinnamic acid and then p-coumaric acid Other forms oflignin monomers are caffeic acid ferulic acid 5-hydroxy-ferulic acid and sinapinic acid [49ndash51] Finallymonomers arepolymerized to form lignin products Monomers of lignin arecategorized into three types syringly lignin (S-lignin) guaia-cyl lignin (G-lignin) and hydroxyphenyl lignin (H-lignin)From the gnome analysis a total of 66 lignin synthesis-related gene families were characterized in P bretschneideriIt signifies the high demand for lignin synthesis in pear [15]In ldquoDangshan Surdquo pulp milled wood lignin was identifiedas guaiacyl-syringyl-lignin It was observed that ldquoDangshanSurdquo lignin possesses more guaiacyl units than the syringylunits [49] Hydroxycinnamoyl transferases (HCT) play asignificant role in the lignin synthesis [52] Accumulation ofG-lignin and S-lignin is interrelated with theHCT expressionespecially at early fruit developmental stage [15]
Cinnamoyl-CoA reductase (CCR) and cinnamyl alco-hol dehydrogenase (CAD) belonging to medium-or-short-chain dehydrogenasereductase are key enzymes for ligninmonomer synthesis [53] Totally 31 CCRs and 26 CADsgenes were identified in P bretschneideri ldquoDangshan Surdquo Allmembers of CCR and CAD identified in P bretschneideri arenot involved in the lignin biosynthesis [54] Among them
PbCAD2 PbCCR1 PbCCR2 and PbCCR3 were identified toparticipate in the lignin synthesis of stone cells [15] NAC(NAM ATAF12 and CUC2) and LIM (Lin11Isl1Mec3) arean important TF influencing the lignin pathway [55 56]Mostof theCCR andCADmembers present in the pear possess SPL(squamosal promoter binding-like) light-responsive elementon their upstream Functions of PbCCR and PbCAD arerelated to the light signaling Presence of MYB-binding ACcis elements in some promoter of the PbCCRs suggestedthat phenylpropanoid metabolism of lignin synthesis wasregulated by MYB transcription factors Similarly TGACG-motif on some PbCCRs and all PbCADrsquos promoter regionsrevealed their involvement in the abscisic acid jasmonicacid andmethyl jasmonic acidmetabolism [15]The pictorialillustration of genesTFs required for the lignin synthesis aswell as stone cell formation is mentioned in Figure 1
There are many internal and external factors involved inthe stone cell formation of pear Identification of candidategenes of lignin biosynthesis and stone cell formation willbe very much useful to improve the cultural practices forproducing pear fruits with different palatable level of stonecells
33 Fruit Aroma and Softness in Strawberry Strawberry iswidely appreciated for its delicate flavor aroma and nutri-tional value Aroma of strawberry is due to esters alcoholsaldehydes and sulfur compounds Hundreds of volatile estershave been correlated with strawberry ripening and aroma
BioMed Research International 7
[57] Volatile esters are the major constituents of floral scentWild species such as F vesca and F virginiana have muchstronger aroma than the cultivated types Compared to theregular octoploid strawberry unique phenolic compoundswere found inF vesca fruits such as taxifolin 3-O-arabinosideand peonidin 3-O-malonylglucoside [58] Pinene synthase(PINS) is primarily expressed in wild strawberry whileinsertional mutation reduced its expression in cultivatedspecies F vesca contains high amounts of ethyl-acetate andlower methyl-butyrate ethyl-butyrate and furanone levels Fnilgerrensis possesses higher ethyl-acetate and furanone butlower methyl-butyrate and ethyl-butyrate Hybrids betweenF vesca and F ananassa have intermediate contents of fra-grance and aroma related compounds while crosses betweenF nilgerrensis and F ananassa more closely resemble Fnilgerrensis [17] Volatile compounds found to be responsiblefor general strawberry smell are 2 5-dimethyl-4-hydroxy-3(2H)-furanone linalool and ethyl hexanoate Neverthelessethyl butanoate methyl butanoate 120574-decalactone and 2-heptanone are represented as cultivar specific aroma com-pounds [59] O-methyltransferase of strawberry (FaOMT) isvital for the biosynthesis of vanillin and furaneol [60]Alcoholacyltransferase (AATs) in strawberry (SAAT) is involved inthe last step of volatile esters synthesis and vital for flavorbiogenesis in ripening fruit SAAT catalyzes esterificationof an acyl moiety from actyl-CoA to alcohol [61] Straw-berry quinone oxidoreductase (FaQR) is required for thebiosynthesis of furaneol Furaneol and its methoxy derivative(methoxyfuraneol and mesifuran) are catalyzed by OMT Allthree furaneol compounds are highly accumulated duringfruit ripening stage [62] Though two types of pyruvatedecarboxylase (PDC) were identified in strawberry onlyFaPDC1 was induced during fruit ripening [63]
Strawberry is highly perishable even with controlledatmospheric storage Higher proportion of fruit last occurreddue to its softness and sensitivity to fungal disease Redcolored strawberry showed the higher level of anthocyanin-related transcripts [64] FcMYB1 could regulate branching-point of the anthocyaninproanthocyanidin biosynthesisFaWRKY1 mediate defense response and FaPE1 encodedfor pectin methyl esterase are conferred at least with apartial resistance of ripened fruit against Botrytis cinerea[65 66] Polygalacturonase 1 of F x ananassa (FaPG1) iscritical for fruit softening [67] In strawberry fruits beta-D-glucosyltransferase (FaGT) correlated with the relevantphenylpropanoid glucosides [68]D-xylose reductase (FaXyl1)and beta-xylosidase activity were higher in ldquoToyonakardquo (soft)than in the ldquoCamarosardquo (firm) showing the correlationbetween FaXyl1 expression and fruit softening [69] Fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase) is involvedin the firmness and postharvest life [70] A lesser activity ofbeta-galactosidase (120573Gal) and 120573Xyl activity were correlatedwith decreased fruit firmness in F chiloensis and F timesananassa respectively [71] Expression of FaCCR is higherin soft fruit cultivar (Gorella) whereas FaCAD is higher infirm fruit cultivar (Holiday) [72] Expression of five expansingenes (FaEXP1 FaEXP2 FaEXP4 FaEXP5 and FaEXP6) wasstudied in cultivars with different firmness ldquoSelvardquo (hard)ldquoCamarosardquo (medium) and ldquoToyonakardquo (soft) Higher level
of FaEXP1 FaEXP2 and FaEXP5 expression was foundin fruit with less firmness (ldquoToyonakardquo) than the othertwo cultivars (ldquoSelvardquo and ldquoCamarosardquo) Fruit firmnessis identified to be associated with pectate lyase (FaPel1)identified Expansin activity was characterized by cell wallmodification [73] Polysaccharides were modified by fivedifferent genes such as FasPG FaPG-like FaPel1 FaPel2 andFaEXP2 [74] Sorbitol dehydrogenase (FaSDH) and sorbitol-6-phosphate dehydrogenase (FaS6PDH) genes are involved withthe sorbitol synthesis in leaves fruits and shoot tips [75]SEPALLATA (SEP)4-like gene FaMADS9 is responsible forthe fruit ripening [76]
Apart from the aesthetic and taste mechanisms of flower-ing and its response to the light signaling in strawberry needto be studied in detail Cultivars with continuous floweringand growing underminimal light energy are beneficial for thestrawberry growers as most of the commercial cultivation iscarried out in the controlled greenhouse
34 Early Blooming and Fruit Ripening in Prunus Prunusis the first plant to bloom in later winterearly spring Soit is the best model plant to study early flowering as wellas chilling tolerance Dehydrins are known as 2 or D-11family late-embryogenesis-abundant (LEA) proteins Theyplay a vital role in plant growth and cold tolerance [77] InP mume 30 LEA genes were characterized and classifiedinto eight groups LEA1 LEA2 LEA3 LEA4 LEA5 PvLEA18dehydrin and seed maturation protein Out of 30 identifiedgenes 22 were expressed in flowers and 19 were inducedby abscisic acid (ABA) treatments [78] Molecular cloningof PmLEA8 PmLEA10 PmLEA19 PmLEA20 and PmLEA29showed that except PmLEA8 all other genes enhancedthe freezing-tolerance Interestingly among all cold-resistantLEA genemembers studied only PmLEA19were upregulatedfour timeswhen the branches of Pmumewere exposed to 4∘C[79]Downregulation inPmume dormancy associatedMADS(PmDAM) 4 PmDAM5 and PmDAM6 expression releasesthe endodormancy [80] Among the six DAM genes exceptPmDAM3 all other genes are responsive to the photoperiodand seasonal (cold) responses [81] In P persica from six iden-tified DAM genes PpDAM5 and PpDAM6 were character-ized to be involved in the lateral bud dormancy breakage [82]DAM5 and DAM6 were identified as homologous to ShortVegetative Phase (SVP)AGL 24 in A thaliana Both SVPand AGL-24 are required for floral meristem identity [83]AGL24 is well known for promoting early flowering and floraltransition in plants [58] Transcriptome analysis betweencold sensitive (ldquoMorettinirdquo) and cold tolerant (ldquoRoyal Gloryrdquo)cultivars in P persica showed that 120573-D-xylosidase (BXL)and pathogen-related protein 4b (PR-4B) were significantlyexpressed only in resistant variety [84] Other candidategenes identified as required to control flowering time aresuppressor of phyA (SPA) COP1 interacting protein8 (CIP8)phytochrome A (phyA) and phytochrome interacting factor 3(PIF3) [85] Figure 2 demonstrates the important key genesinvolved in cold tolerance early blooming and floweringtime control of P mume Higher number of aesthetic prop-erties related genes such as benzyl alcohol acetyltransferase(BEAT) (34) are identified in P mume Only 16 in Malus x
8 BioMed Research International
PmLEA19 PmDAM4 PmDAM5 and PmDAM6
SPA CIP8 phyA and PIF3BXL and PR-4B
Cold toler
ance
Cold tolerance
Control flowering time
Dorman
cy re
lease
Figure 2 Factors involved in the early blooming of Chinese plumJapanese apricot Prunus meme Pm late-embryogenesis-abundant LEAdormancy associated MADS DAM 120573-D-xylosidase BXL pathogen-related protein 4b PR-4B suppressor of phyA SPA COP1 interactingprotein8 CIP8 phytochrome A phyA and phytochrome interacting factor3 PIF3 The lower arrow represents downregulation
domestica 14 in F vesca 4 inVitis vinifera 17 in P trichocarpaand 3 inA thaliana of BEAT genes were identifiedThereforein P mume BEAT genes are considered as key factor todetermine its exclusive floral fragrance [23]
In Prunus UDP-glucose-flavonoid-3-O-glucosyltransfer-ase (UFGT) expression was higher during the initial periodand it is reduced on the developmental process Duringthe ripening processMYB10 MYB123 and basic-helix-loop-helix (bHLH3)were upregulatedwhereasMYB16 andMYB111were downregulated Higher anthocyanin and Proantho-cyanidin levels were correlatedwith theMYB10 andMYBPA1respectively Stimulation of TFs is responsive for the devel-opment and external stimuli [86] Gene encoding ethylene-responsive transcription factor (ERF)4 is necessary for the fruitmaturity [87] Though 74 EFR genes were predicted in thepeach genome only one copy of ERF4 has existed ThereforeERF4 is vital to control the fruit maturity and ripening inpeach [85] An initial stage of fruit has higher aldehyde andalcohol production whereas later stages have lesser contentwhich is correlated with the ester production Abundance ofalcohol dehydrogenase (ADH) and lipoxygenase (LOX) geneis constant in the fruit development stages Expression ofAATwas sharply increased in the later stage of harvest [88] Rapidsoftening of fruits was related to the ethylene productionin P persica It is correlated with expression of PpACS1 (1-aminocyclopropane-1-carboxylic acid synthase) [89] Ripenedsweet cherry P avium has unique fragrance In the sweetcherry (ldquoHongdengrdquo ldquoHongyanrdquo and ldquoRainierrdquo) 97 volatilecompounds were identified Alcohols and terpenes were thepredominant components of bound volatiles Benzyl alcoholgeraniol and 2-phenylethanol are the major bound volatileconstituents Free volatile compounds majorly present insweet cherry are hexanal 2-hexenal 2-hexen-1-ol benzyl
alcohol and benzaldehyde Free volatiles are responsible forfloral aroma and bound volatiles involved in fruit freshnessDepending on the level of free and bound volatiles aroma andglycosidically bound compounds aroma and fruit firmnesswere varied between the cultivars of sweet cherry [90]
In Prunus apricot peach sweet cherry and sour cherryare widely used for human consumption Comparativegenomics study between the species offer the candidate geneto produce hybrids with more preferable qualities
35 Blooming and Scent Pathways in Rose Continuous flow-ering (CF)recurrent blooming (RB) genotypes flowers in allfavorable seasons whereas once-flowering (OF) genotypesonly flowers in spring Recurrent blooming is an importanttrait required by breeders R x hybrida ldquoLa Francerdquo was thefirst hybrid combined with the growth vigor of Europeanspecies and recurrent blooming of Chinese species It hasthe complex genetic pool combination of three ancestralgenotypes such as Cinnamomeae Synstylae and ChinensesInsertion of TE in the TFL1 encodes gene Ksncopia (KSN)was found as responsible for the recurrent blooming of ldquoLaFrancerdquo [30] Previously Horibe et al (2013) reported thatKSN gene regulates the CF behavior of R rugosa [91] Wanget al (2012) studied recurrent flowering character and theexpression patterns of TFL1 homologs in R multiflora Rrugosa R chinensis and other speciescultivars Among thethree orthologs RTFL1c was highly expressed at all fourflowering stages in R multiflora and R rugosa (nonrecurrentflowering species) and barely detected in R chinensis (arecurrent flowering species) at any stage Therefore it can beconsidered that lower expression of RTFL1c is required forrecurrent flowering of roses [92] Iwata et al (2012) elucidatethat occurrence of TE insertion and point mutation in the
BioMed Research International 9
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
[57] Volatile esters are the major constituents of floral scentWild species such as F vesca and F virginiana have muchstronger aroma than the cultivated types Compared to theregular octoploid strawberry unique phenolic compoundswere found inF vesca fruits such as taxifolin 3-O-arabinosideand peonidin 3-O-malonylglucoside [58] Pinene synthase(PINS) is primarily expressed in wild strawberry whileinsertional mutation reduced its expression in cultivatedspecies F vesca contains high amounts of ethyl-acetate andlower methyl-butyrate ethyl-butyrate and furanone levels Fnilgerrensis possesses higher ethyl-acetate and furanone butlower methyl-butyrate and ethyl-butyrate Hybrids betweenF vesca and F ananassa have intermediate contents of fra-grance and aroma related compounds while crosses betweenF nilgerrensis and F ananassa more closely resemble Fnilgerrensis [17] Volatile compounds found to be responsiblefor general strawberry smell are 2 5-dimethyl-4-hydroxy-3(2H)-furanone linalool and ethyl hexanoate Neverthelessethyl butanoate methyl butanoate 120574-decalactone and 2-heptanone are represented as cultivar specific aroma com-pounds [59] O-methyltransferase of strawberry (FaOMT) isvital for the biosynthesis of vanillin and furaneol [60]Alcoholacyltransferase (AATs) in strawberry (SAAT) is involved inthe last step of volatile esters synthesis and vital for flavorbiogenesis in ripening fruit SAAT catalyzes esterificationof an acyl moiety from actyl-CoA to alcohol [61] Straw-berry quinone oxidoreductase (FaQR) is required for thebiosynthesis of furaneol Furaneol and its methoxy derivative(methoxyfuraneol and mesifuran) are catalyzed by OMT Allthree furaneol compounds are highly accumulated duringfruit ripening stage [62] Though two types of pyruvatedecarboxylase (PDC) were identified in strawberry onlyFaPDC1 was induced during fruit ripening [63]
Strawberry is highly perishable even with controlledatmospheric storage Higher proportion of fruit last occurreddue to its softness and sensitivity to fungal disease Redcolored strawberry showed the higher level of anthocyanin-related transcripts [64] FcMYB1 could regulate branching-point of the anthocyaninproanthocyanidin biosynthesisFaWRKY1 mediate defense response and FaPE1 encodedfor pectin methyl esterase are conferred at least with apartial resistance of ripened fruit against Botrytis cinerea[65 66] Polygalacturonase 1 of F x ananassa (FaPG1) iscritical for fruit softening [67] In strawberry fruits beta-D-glucosyltransferase (FaGT) correlated with the relevantphenylpropanoid glucosides [68]D-xylose reductase (FaXyl1)and beta-xylosidase activity were higher in ldquoToyonakardquo (soft)than in the ldquoCamarosardquo (firm) showing the correlationbetween FaXyl1 expression and fruit softening [69] Fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase) is involvedin the firmness and postharvest life [70] A lesser activity ofbeta-galactosidase (120573Gal) and 120573Xyl activity were correlatedwith decreased fruit firmness in F chiloensis and F timesananassa respectively [71] Expression of FaCCR is higherin soft fruit cultivar (Gorella) whereas FaCAD is higher infirm fruit cultivar (Holiday) [72] Expression of five expansingenes (FaEXP1 FaEXP2 FaEXP4 FaEXP5 and FaEXP6) wasstudied in cultivars with different firmness ldquoSelvardquo (hard)ldquoCamarosardquo (medium) and ldquoToyonakardquo (soft) Higher level
of FaEXP1 FaEXP2 and FaEXP5 expression was foundin fruit with less firmness (ldquoToyonakardquo) than the othertwo cultivars (ldquoSelvardquo and ldquoCamarosardquo) Fruit firmnessis identified to be associated with pectate lyase (FaPel1)identified Expansin activity was characterized by cell wallmodification [73] Polysaccharides were modified by fivedifferent genes such as FasPG FaPG-like FaPel1 FaPel2 andFaEXP2 [74] Sorbitol dehydrogenase (FaSDH) and sorbitol-6-phosphate dehydrogenase (FaS6PDH) genes are involved withthe sorbitol synthesis in leaves fruits and shoot tips [75]SEPALLATA (SEP)4-like gene FaMADS9 is responsible forthe fruit ripening [76]
Apart from the aesthetic and taste mechanisms of flower-ing and its response to the light signaling in strawberry needto be studied in detail Cultivars with continuous floweringand growing underminimal light energy are beneficial for thestrawberry growers as most of the commercial cultivation iscarried out in the controlled greenhouse
34 Early Blooming and Fruit Ripening in Prunus Prunusis the first plant to bloom in later winterearly spring Soit is the best model plant to study early flowering as wellas chilling tolerance Dehydrins are known as 2 or D-11family late-embryogenesis-abundant (LEA) proteins Theyplay a vital role in plant growth and cold tolerance [77] InP mume 30 LEA genes were characterized and classifiedinto eight groups LEA1 LEA2 LEA3 LEA4 LEA5 PvLEA18dehydrin and seed maturation protein Out of 30 identifiedgenes 22 were expressed in flowers and 19 were inducedby abscisic acid (ABA) treatments [78] Molecular cloningof PmLEA8 PmLEA10 PmLEA19 PmLEA20 and PmLEA29showed that except PmLEA8 all other genes enhancedthe freezing-tolerance Interestingly among all cold-resistantLEA genemembers studied only PmLEA19were upregulatedfour timeswhen the branches of Pmumewere exposed to 4∘C[79]Downregulation inPmume dormancy associatedMADS(PmDAM) 4 PmDAM5 and PmDAM6 expression releasesthe endodormancy [80] Among the six DAM genes exceptPmDAM3 all other genes are responsive to the photoperiodand seasonal (cold) responses [81] In P persica from six iden-tified DAM genes PpDAM5 and PpDAM6 were character-ized to be involved in the lateral bud dormancy breakage [82]DAM5 and DAM6 were identified as homologous to ShortVegetative Phase (SVP)AGL 24 in A thaliana Both SVPand AGL-24 are required for floral meristem identity [83]AGL24 is well known for promoting early flowering and floraltransition in plants [58] Transcriptome analysis betweencold sensitive (ldquoMorettinirdquo) and cold tolerant (ldquoRoyal Gloryrdquo)cultivars in P persica showed that 120573-D-xylosidase (BXL)and pathogen-related protein 4b (PR-4B) were significantlyexpressed only in resistant variety [84] Other candidategenes identified as required to control flowering time aresuppressor of phyA (SPA) COP1 interacting protein8 (CIP8)phytochrome A (phyA) and phytochrome interacting factor 3(PIF3) [85] Figure 2 demonstrates the important key genesinvolved in cold tolerance early blooming and floweringtime control of P mume Higher number of aesthetic prop-erties related genes such as benzyl alcohol acetyltransferase(BEAT) (34) are identified in P mume Only 16 in Malus x
8 BioMed Research International
PmLEA19 PmDAM4 PmDAM5 and PmDAM6
SPA CIP8 phyA and PIF3BXL and PR-4B
Cold toler
ance
Cold tolerance
Control flowering time
Dorman
cy re
lease
Figure 2 Factors involved in the early blooming of Chinese plumJapanese apricot Prunus meme Pm late-embryogenesis-abundant LEAdormancy associated MADS DAM 120573-D-xylosidase BXL pathogen-related protein 4b PR-4B suppressor of phyA SPA COP1 interactingprotein8 CIP8 phytochrome A phyA and phytochrome interacting factor3 PIF3 The lower arrow represents downregulation
domestica 14 in F vesca 4 inVitis vinifera 17 in P trichocarpaand 3 inA thaliana of BEAT genes were identifiedThereforein P mume BEAT genes are considered as key factor todetermine its exclusive floral fragrance [23]
In Prunus UDP-glucose-flavonoid-3-O-glucosyltransfer-ase (UFGT) expression was higher during the initial periodand it is reduced on the developmental process Duringthe ripening processMYB10 MYB123 and basic-helix-loop-helix (bHLH3)were upregulatedwhereasMYB16 andMYB111were downregulated Higher anthocyanin and Proantho-cyanidin levels were correlatedwith theMYB10 andMYBPA1respectively Stimulation of TFs is responsive for the devel-opment and external stimuli [86] Gene encoding ethylene-responsive transcription factor (ERF)4 is necessary for the fruitmaturity [87] Though 74 EFR genes were predicted in thepeach genome only one copy of ERF4 has existed ThereforeERF4 is vital to control the fruit maturity and ripening inpeach [85] An initial stage of fruit has higher aldehyde andalcohol production whereas later stages have lesser contentwhich is correlated with the ester production Abundance ofalcohol dehydrogenase (ADH) and lipoxygenase (LOX) geneis constant in the fruit development stages Expression ofAATwas sharply increased in the later stage of harvest [88] Rapidsoftening of fruits was related to the ethylene productionin P persica It is correlated with expression of PpACS1 (1-aminocyclopropane-1-carboxylic acid synthase) [89] Ripenedsweet cherry P avium has unique fragrance In the sweetcherry (ldquoHongdengrdquo ldquoHongyanrdquo and ldquoRainierrdquo) 97 volatilecompounds were identified Alcohols and terpenes were thepredominant components of bound volatiles Benzyl alcoholgeraniol and 2-phenylethanol are the major bound volatileconstituents Free volatile compounds majorly present insweet cherry are hexanal 2-hexenal 2-hexen-1-ol benzyl
alcohol and benzaldehyde Free volatiles are responsible forfloral aroma and bound volatiles involved in fruit freshnessDepending on the level of free and bound volatiles aroma andglycosidically bound compounds aroma and fruit firmnesswere varied between the cultivars of sweet cherry [90]
In Prunus apricot peach sweet cherry and sour cherryare widely used for human consumption Comparativegenomics study between the species offer the candidate geneto produce hybrids with more preferable qualities
35 Blooming and Scent Pathways in Rose Continuous flow-ering (CF)recurrent blooming (RB) genotypes flowers in allfavorable seasons whereas once-flowering (OF) genotypesonly flowers in spring Recurrent blooming is an importanttrait required by breeders R x hybrida ldquoLa Francerdquo was thefirst hybrid combined with the growth vigor of Europeanspecies and recurrent blooming of Chinese species It hasthe complex genetic pool combination of three ancestralgenotypes such as Cinnamomeae Synstylae and ChinensesInsertion of TE in the TFL1 encodes gene Ksncopia (KSN)was found as responsible for the recurrent blooming of ldquoLaFrancerdquo [30] Previously Horibe et al (2013) reported thatKSN gene regulates the CF behavior of R rugosa [91] Wanget al (2012) studied recurrent flowering character and theexpression patterns of TFL1 homologs in R multiflora Rrugosa R chinensis and other speciescultivars Among thethree orthologs RTFL1c was highly expressed at all fourflowering stages in R multiflora and R rugosa (nonrecurrentflowering species) and barely detected in R chinensis (arecurrent flowering species) at any stage Therefore it can beconsidered that lower expression of RTFL1c is required forrecurrent flowering of roses [92] Iwata et al (2012) elucidatethat occurrence of TE insertion and point mutation in the
BioMed Research International 9
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
Figure 2 Factors involved in the early blooming of Chinese plumJapanese apricot Prunus meme Pm late-embryogenesis-abundant LEAdormancy associated MADS DAM 120573-D-xylosidase BXL pathogen-related protein 4b PR-4B suppressor of phyA SPA COP1 interactingprotein8 CIP8 phytochrome A phyA and phytochrome interacting factor3 PIF3 The lower arrow represents downregulation
domestica 14 in F vesca 4 inVitis vinifera 17 in P trichocarpaand 3 inA thaliana of BEAT genes were identifiedThereforein P mume BEAT genes are considered as key factor todetermine its exclusive floral fragrance [23]
In Prunus UDP-glucose-flavonoid-3-O-glucosyltransfer-ase (UFGT) expression was higher during the initial periodand it is reduced on the developmental process Duringthe ripening processMYB10 MYB123 and basic-helix-loop-helix (bHLH3)were upregulatedwhereasMYB16 andMYB111were downregulated Higher anthocyanin and Proantho-cyanidin levels were correlatedwith theMYB10 andMYBPA1respectively Stimulation of TFs is responsive for the devel-opment and external stimuli [86] Gene encoding ethylene-responsive transcription factor (ERF)4 is necessary for the fruitmaturity [87] Though 74 EFR genes were predicted in thepeach genome only one copy of ERF4 has existed ThereforeERF4 is vital to control the fruit maturity and ripening inpeach [85] An initial stage of fruit has higher aldehyde andalcohol production whereas later stages have lesser contentwhich is correlated with the ester production Abundance ofalcohol dehydrogenase (ADH) and lipoxygenase (LOX) geneis constant in the fruit development stages Expression ofAATwas sharply increased in the later stage of harvest [88] Rapidsoftening of fruits was related to the ethylene productionin P persica It is correlated with expression of PpACS1 (1-aminocyclopropane-1-carboxylic acid synthase) [89] Ripenedsweet cherry P avium has unique fragrance In the sweetcherry (ldquoHongdengrdquo ldquoHongyanrdquo and ldquoRainierrdquo) 97 volatilecompounds were identified Alcohols and terpenes were thepredominant components of bound volatiles Benzyl alcoholgeraniol and 2-phenylethanol are the major bound volatileconstituents Free volatile compounds majorly present insweet cherry are hexanal 2-hexenal 2-hexen-1-ol benzyl
alcohol and benzaldehyde Free volatiles are responsible forfloral aroma and bound volatiles involved in fruit freshnessDepending on the level of free and bound volatiles aroma andglycosidically bound compounds aroma and fruit firmnesswere varied between the cultivars of sweet cherry [90]
In Prunus apricot peach sweet cherry and sour cherryare widely used for human consumption Comparativegenomics study between the species offer the candidate geneto produce hybrids with more preferable qualities
35 Blooming and Scent Pathways in Rose Continuous flow-ering (CF)recurrent blooming (RB) genotypes flowers in allfavorable seasons whereas once-flowering (OF) genotypesonly flowers in spring Recurrent blooming is an importanttrait required by breeders R x hybrida ldquoLa Francerdquo was thefirst hybrid combined with the growth vigor of Europeanspecies and recurrent blooming of Chinese species It hasthe complex genetic pool combination of three ancestralgenotypes such as Cinnamomeae Synstylae and ChinensesInsertion of TE in the TFL1 encodes gene Ksncopia (KSN)was found as responsible for the recurrent blooming of ldquoLaFrancerdquo [30] Previously Horibe et al (2013) reported thatKSN gene regulates the CF behavior of R rugosa [91] Wanget al (2012) studied recurrent flowering character and theexpression patterns of TFL1 homologs in R multiflora Rrugosa R chinensis and other speciescultivars Among thethree orthologs RTFL1c was highly expressed at all fourflowering stages in R multiflora and R rugosa (nonrecurrentflowering species) and barely detected in R chinensis (arecurrent flowering species) at any stage Therefore it can beconsidered that lower expression of RTFL1c is required forrecurrent flowering of roses [92] Iwata et al (2012) elucidatethat occurrence of TE insertion and point mutation in the
BioMed Research International 9
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
TFL1 ortholog on rose and strawberry correlate with recur-rent blooming [93] Higher expression of TFL1 in seasonalflower is associated with the repression of LEAFY (LFY) andactivating protein-1 (AP1) a downstream gene of FT [94]Expression of flowering locus T of rose (RoFT) was pro-gressively increased after floral bud formation CONSTANSTF induces the FT and upon induction FT was suggestedto move from leaves to shoot apical meristem (SAM) viaphloem [95ndash97] Additionally suppressor of Ty (SPT) anddelay of germination (DOG)1 are other important candidatesdetermining recurrent blooming in roses [31]
Rose scent is a complex trait involved with hundredsof volatile molecules Rose floral scent contains phenolicderivatives terpenoids and fatty acid derivatives Severalgenes have been identified to be related to rose scent pro-duction Floral scent of roses contains higher germacreneD synthase Cyanidin and germacrene D were identified tobe involved in the color and scent pathways Sesquiterpenesynthase catalyzes the production of germacrene D [98]Phenylacetaldehyde synthase (PAAS) and phenylacetaldehydereductase (PAR) are responsible for the synthesis of 2-phenylethyl alcohol a typical rose scent compound [99]Anthocyanin synthesis on rose was linked with the pig-mentation and volatile (scent) compounds related pathwaysAnthocyanin and volatile compound have been generatedby enabling the formation of MYB-bHLH-WD40 proteincomplex Orcinol-o-methyltransferase (RhOOMT) 1 and 2 isresponsible for synthesis of 2OMT Alcohol acyltransferaseof R hybrida (RhAAT1) gene converts alcohol geraniol intogeranyl acetate [62] Major scent compound of Euro-pean roses is 2-phenylethanol and monoterpenes [100 101]RhOOMTs catalyze the orcinol to synthesize two importantvolatiles such as 35-dimethoxy toluene (DMT) and 135-metoxy benzene (TMB) biosynthesis in R hybrida [62]From the study of interhybrid cultivars of rose DMT wasconcluded to come from Chinese rose as ancient Europeanroses such as R damascena and R gallica do not produceDMT [102] Geraniol a hydrolyzed product and its down-stream monoterpene volatile metabolites are responsiblefor the aroma of rose petals Nudix hydrolase (NUDX)1 isinvolved in synthesis of geraniol and other geraniol-derivedmonoterpenes [103] Still there are many pathways rose scentneed to be elucidated
Genome released in rose will be helpful for decodingthe metabolic networks of scent pathway floral transitionand flowering pattern Therefore irrespective of complex andcumbersome heterozygous nature interspecific hybridiza-tion can be accelerated to produce hybrid with valuable traitsin rose
4 Conclusions
Complete genome information of plant reduces effort andtime required for conventional MAS approach Identificationand characterization of genes controlling important traits andtaggingmolecularmarkers for introgression to produce a newvariety are feasible with available genome information Alongwith abiotic and biotic stress resistance several fruit qualitytraits can be improved with genomics-based studies Fruit
firmness is one of the desirable quality traits It depends onthe postharvest shelf life cell turgor pressure and intrinsiccharacteristics of the cell wall Modification and turnoverof the primary cell wall are required for both size andsoftness of fruits New varietiescultivars with smalllargersize good-flavored fruits attractive color sugar and acidlevels reduced juvenile phase massive and constant yieldsreduced susceptibility to fruit cracking self-compatibilityand improved resistance or tolerance to disease are nowfeasible with the completion of the whole genome sequence
Conflicts of Interest
The authors declare that they have no conflicts of interest
References
[1] D Potter T Eriksson R C Evans et al ldquoPhylogeny andclassification of Rosaceaerdquo Plant Systematics and Evolution vol266 no 1-2 pp 5ndash43 2007
[2] V Shulaev S S Korban B Sosinski et al ldquoMultiple models forRosaceae genomicsrdquo Plant Physiology vol 147 no 3 pp 985ndash1003 2008
[3] D Potter F Gao P E Bortiri S-H Oh and S BaggettldquoPhylogenetic relationships in Rosaceae inferred from chloro-plast matK and trnL-trnF nucleotide sequence datardquo PlantSystematics and Evolution vol 231 no 1ndash4 pp 77ndash89 2002
[4] C S Pareek R Smoczynski and A Tretyn ldquoSequencing tech-nologies and genome sequencingrdquo Journal of Applied Geneticsvol 52 no 4 pp 413ndash435 2011
[5] A G Day-Williams and E Zeggini ldquoThe effect of next-gen-eration sequencing technology on complex trait researchrdquoEuropean Journal of Clinical Investigation vol 41 no 5 pp 561ndash567 2011
[6] N Daccord J-M Celton G Linsmith et al ldquoHigh-quality denovo assembly of the apple genome and methylome dynamicsof early fruit developmentrdquo Nature Genetics vol 49 no 7 pp1099ndash1106 2017
[7] J Stapley J Reger P G D Feulner et al ldquoAdaptation genomicsthe next generationrdquo Trends in Ecology and Evolution vol 25no 12 pp 705ndash712 2010
[8] M Kellerhals ldquoIntroduction to Apple (Malus x domestica)rdquo inGenetics and Genomics of Rosaceae S E G Kevin andM FoltaEds pp 73ndash84 2009
[9] A Cornille P Gladieux M J M Smulders et al ldquoNew insightinto the history of domesticated apple Secondary contributionof the European wild apple to the genome of cultivated vari-etiesrdquo PLoS Genetics vol 8 article e1002703 2012
[10] A Cornille T Giraud M J M Smulders I Roldan-Ruiz andP Gladieux ldquoThe domestication and evolutionary ecology ofapplesrdquo Trends in Genetics vol 30 no 2 pp 57ndash65 2014
[11] R Velasco A Zharkikh and J Affourtit ldquoThe genome ofthe domesticated apple (Malus times domestica Borkh)rdquo NatureGenetics vol 42 no 10 pp 833ndash839 2010
[12] X Li L Kui J Zhang et al ldquoImproved hybrid de novogenome assembly of domesticated apple (Malus x domestica)rdquoGigaScience vol 5 article 35 2016
[13] G Rubtsov ldquoGeographical distribution of the genus Pyrus andtrends and factors in its evolutionrdquoTheAmericanNaturalist vol78 pp 358ndash366 1944
10 BioMed Research International
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
[14] T Saito ldquoAdvances in Japanese pear breeding in JapanrdquoBreedingScience vol 66 no 1 pp 46ndash59 2016
[15] J Wu Z Wang Z Shi et al ldquoThe genome of the pear (Pyrusbretschneideri Rehd)rdquoGenomeResearch vol 23 no 2 pp 396ndash408 2013
[16] D Chagne R N CrowhurstM Pindo et al ldquoThe draft genomesequence of European pear (Pyrus communis L lsquoBartlettrsquo)rdquoPLoS ONE vol 9 article e92644 2014
[17] K EHummer and JHancock ldquoStrawberry genomics botanicalhistory cultivation traditional breeding and new technolo-giesrdquo in Genetics and Genomics of Rosaceae pp 413ndash435Springer 2009
[18] O Darwish J P Slovin C Kang et al ldquoSGR an online genomicresource for the woodland strawberryrdquo BMC Plant Biology vol13 article 223 2013
[19] V Shulaev D J Sargent R N Crowhurst et al ldquoThe genomeof woodland strawberry (Fragaria vesca)rdquo Nature Genetics vol43 no 2 pp 109ndash116 2011
[20] H Hirakawa K Shirasawa S Kosugi et al ldquoDissection ofthe octoploid strawberry genome by deep sequencing of thegenomes of fragaria speciesrdquo DNA Research vol 21 no 2 pp169ndash181 2014
[21] J Shi J Gong J Liu XWu andY Zhang ldquoAntioxidant capacityof extract from edible flowers of Prunusmume in China and itsactive componentsrdquo LWT- Food Science and Technology vol 42no 2 pp 477ndash482 2009
[22] S Fan D G Bielenberg T N Zhebentyayeva et al ldquoMappingquantitative trait loci associatedwith chilling requirement heatrequirement and bloom date in peach (Prunus persica)rdquo NewPhytologist vol 185 no 4 pp 917ndash930 2010
[23] Q Zhang W Chen L Sun Z Danyang and W Zeng ldquoThegenome of Prunus mumerdquoNature vol 3 article 1318 2012
[24] K G D Bielenberg and J X Chaparro ldquoAn introduction topeach (Prunus persica)rdquo in Genetics and Genomics of RosaceaeS E G Kevin and M Folta Eds pp 223ndash234 2009
[25] I Verde A G Abbott S Scalabrin et al ldquoThe high-quality draftgenome of peach (Prunus persica) identifies unique patterns ofgenetic diversity domestication and genome evolutionrdquoNatureGenetics vol 45 no 5 pp 487ndash494 2013
[26] I Verde J Jenkins L Dondini et al ldquoThe Peach v20release high-resolution linkage mapping and deep resequenc-ing improve chromosome-scale assembly and contiguityrdquo BMCGenomics vol 18 article 225 2017
[27] J C E Dirlewanger and A F Iezzoni ldquoAna wiinsch sweetand sour cherries linkage mapsrdquo in Genetics and Genomics ofRosaceae S E G Kevin and M Folta Eds pp 291ndash314 2009
[28] K Shirasawa K Isuzugawa M Ikenaga et al ldquoThe genomesequence of sweet cherry (Prunus avium) for use in genomics-assisted breedingrdquo DNA Research vol 24 no 5 pp 499ndash5082017
[29] H Nybom ldquoIntroduction to rosardquo in Genetics and Genomics ofRosaceae pp 339ndash351 Springer 2009
[30] O Raymond J Gouzy J Just et al ldquoThe Rosa genome providesnew insights into the domestication of modern rosesrdquo NatureGenetics vol 50 pp 772ndash777 2018
[31] L H Saint-Oyant T Ruttink L Hamama et al ldquoA high-qualitygenome sequence of Rosa chinensis to elucidate ornamentaltraitsrdquo Nature plants article 1 2018
[32] C Hurst ldquoNotes on the origin and evolution of our gardenrosesrdquo Journal of the Horticultural Society vol 66 pp 282ndash2891941
[33] D Terefe-Ayana A Yasmin T L Le et al ldquoMining disease-resistance genes in roses functional and molecular characteri-zation of the rdr1 locusrdquo Frontiers in Plant Science vol 2 article35 2011
[34] N Nakamura H Hirakawa S Sato et al ldquoGenome structureof Rosa multiflora a wild ancestor of cultivated rosesrdquo DNAResearch vol 25 no 2 pp 113ndash121 2017
[35] N Mimida S-I Kidou and N Kotoda ldquoConstitutive expres-sion of two apple (Malus x domestica Borkh) homolog genesof LIKE HETEROCHROMATIN PROTEIN1 affects floweringtime andwhole-plant growth in transgenic ArabidopsisrdquoMolec-ular Genetics and Genomics vol 278 no 3 pp 295ndash305 2007
[36] N Kotoda H Hayashi M Suzuki et al ldquoMolecular charac-terization of flowering LOCUS t-like genes of apple (malus timesdomestica borkh)rdquo Plant amp Cell Physiology (PCP) vol 51 no4 pp 561ndash575 2010
[37] C Spruck H Strohmaier M Watson et al ldquoA CDK-independ-ent function of mammalian Cks1 targeting of SCFSkp2 to theCDK inhibitor p27Kip1rdquo Molecular Cell vol 7 no 3 pp 639ndash650 2001
[38] C Ferrandiz S Pelaz and M F Yanofsky ldquoControl of carpeland fruit development in Arabidopsisrdquo Annual Review ofBiochemistry vol 68 pp 321ndash354 1999
[39] B J Janssen K Thodey R J Schaffer et al ldquoGlobal geneexpression analysis of apple fruit development from the floralbud to ripe fruitrdquo BMC Plant Biology vol 8 article 16 2008
[40] V Cevik C D Ryder A Popovich K Manning G J Kingand G B Seymour ldquoA FRUITFULL-like gene is associatedwith genetic variation for fruit flesh firmness in apple (Malusdomestica Borkh)rdquo Tree Genetics and Genomes vol 6 no 2pp 271ndash279 2010
[41] F Devoghalaere T Doucen B Guitton et al ldquoA genomicsapproach to understanding the role of auxin in apple (Malus xdomestica) fruit size controlrdquo BMC Plant Biology vol 12 article7 2012
[42] M Li F Feng and L Cheng ldquoExpression patterns of genesinvolved in sugar metabolism and accumulation during applefruit developmentrdquo PLoS ONE vol 7 article e33055 2012
[43] M Nosarzewski and D D Archbold ldquoTissue-specific expres-sion of sorbitol dehydrogenase in apple fruit during earlydevelopmentrdquo Journal of Experimental Botany vol 58 no 7 pp1863ndash1872 2007
[44] P Brookfield P Murphy R Harker and E MacRae ldquoStarchdegradation and starch pattern indices interpretation andrelationship to maturityrdquo Postharvest Biology and Technologyvol 11 no 1 pp 23ndash30 1997
[45] F Costa C P Peace S Stella et al ldquoQTL dynamics forfruit firmness and softening around an ethylene-dependentpolygalacturonase gene in apple (MalusXdomestica Borkh)rdquoJournal of Experimental Botany vol 61 no 11 pp 3029ndash30392010
[46] R G Atkinson P W Sutherland S L Johnston et al ldquoDown-regulation of POLYGALACTURONASE1 alters firmness ten-sile strength and water loss in apple (Malus x domestica) fruitrdquoBMC Plant Biology vol 12 article 129 2012
[47] A M Takos F W Jaffe S R Jacob J Bogs S P Robinson andA R Walker ldquoLight-induced expression of a MYB gene regu-lates anthocyanin biosynthesis in red applesrdquo Plant Physiologyvol 142 no 3 pp 1216ndash1232 2006
[48] C Maliepaard F H Alston G Van Arkel et al ldquoAligning maleand female linkage maps of apple (Malus pumila Mill) using
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
[49] Y Cai G Li J Nie et al ldquoStudy of the structure and biosyntheticpathway of lignin in stone cells of pearrdquo Scientia Horticulturaevol 125 no 3 pp 374ndash379 2010
[50] H Meyermans K Morreel C Lapierre et al ldquoModifica-tions in lignin and accumulation of phenolic glucosides inpoplar xylemupon down-regulation of caffeoyl-coenzymeAO-methyltransferase an enzyme involved in lignin biosynthesisrdquoThe Journal of Biological Chemistry vol 275 no 47 pp 36899ndash36909 2000
[51] J M Humphreys and C Chapple ldquoRewriting the ligninroadmaprdquo Current Opinion in Plant Biology vol 5 no 3 pp224ndash229 2002
[52] L Hoffmann S Besseau P Geoffroy et al ldquoSilencing ofhydroxycinnamoyl-coenzyme A shikimatequinate hydrox-ycinnamoyltransferase affects phenylpropanoid biosynthesisrdquoThe Plant Cell vol 16 no 6 pp 1446ndash1465 2004
[53] X Cheng M Li D Li et al ldquoCharacterization and analysisof CCR and CAD gene families at the whole-genome level forlignin synthesis of stone cells in pear (Pyrus bretschneideri)fruitrdquo Biology Open vol 6 no 11 pp 1602ndash1613 2017
[54] J Thevenin B Pollet B Letarnec et al ldquoThe simultaneousrepression of CCR and CAD two enzymes of the lignin biosyn-thetic pathway results in sterility and dwarfism in ArabidopsisthalianardquoMolecular Plant vol 4 no 1 pp 70ndash82 2011
[55] R ZhongTDemura andZ-HYe ldquoSND1 aNACdomain tran-scription factor is a key regulator of secondary wall synthesis infibers of Arabidopsisrdquo The Plant Cell vol 18 no 11 pp 3158ndash3170 2006
[56] A Kawaoka P Kaothien K Yoshida S Endo K Yamadaand H Ebinuma ldquoFunctional analysis of tobacco LIM proteinNtlim1 involved in lignin biosynthesisrdquo The Plant Journal vol22 no 4 pp 289ndash301 2000
[57] D J Sargent T M Davis and D W Simpson ldquoStrawberry(Fragaria spp) structural genomicsrdquo in Genetics and genomicsof Rosaceae pp 437ndash456 Springer 2009
[58] J Sun X Liu T Yang J Slovin and P Chen ldquoProfilingpolyphenols of two diploid strawberry (Fragaria vesca) inbredlines using UHPLC-HRMSnrdquo Food Chemistry vol 146 pp289ndash298 2014
[59] M Larsen L Poll and C E Olsen ldquoEvaluation of the aromacomposition of some strawberry (Fragaria ananassa Duch)cultivars by use of odour threshold valuesrdquo Zeitschrift furLebensmittel-Untersuchung und -Forschung vol 195 no 6 pp536ndash539 1992
[60] M Wein N Lavid S Lunkenbein E Lewinsohn W Schwaband R Kaldenhoff ldquoIsolation cloning and expression of amultifunctional O-methyltransferase capable of forming 25-dimethyl-4-methoxy-3(2H)-furanone one of the key aromacompounds in strawberry fruitsrdquoThe Plant Journal vol 31 no6 pp 755ndash765 2002
[61] A Aharoni L C P Keizer H J Bouwmeester et al ldquoIdentifica-tion of the SAAT gene involved in strawberry flavor biogenesisby use of DNA microarraysrdquo The Plant Cell vol 12 no 5 pp647ndash661 2000
[62] N Lavid J Wang M Shalit et al ldquoO-methyltransferasesinvolved in the biosynthesis of volatile phenolic derivatives inrose petalsrdquoPlant Physiology vol 129 no 4 pp 1899ndash1907 2002
[63] E Moyano S Encinas-Villarejo J A Lopez-Raez et al ldquoCom-parative study between two strawberry pyruvate decarboxylase
genes along fruit development and ripening post-harvest andstress conditionsrdquo Journal of Plant Sciences vol 166 no 4 pp835ndash845 2004
[64] A Salvatierra P Pimentel M A Moya-Leon P D S Caligariand R Herrera ldquoComparison of transcriptional profiles offlavonoid genes and anthocyanin contents during fruit devel-opment of two botanical forms of Fragaria chiloensis sspchiloensisrdquo Phytochemistry vol 71 no 16 pp 1839ndash1847 2010
[65] S Encinas-Villarejo A M Maldonado F Amil-Ruiz et alldquoEvidence for a positive regulatory role of strawberry (Fragariatimes ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteinsin resistancerdquo Journal of Experimental Botany vol 60 no 11 pp3043ndash3065 2009
[66] S Osorio A Bombarely P Giavalisco et al ldquoDemethylation ofoligogalacturonides by FaPE1 in the fruits of thewild strawberryFragaria vesca triggers metabolic and transcriptional changesassociated with defence and development of the fruitrdquo Journalof Experimental Botany vol 62 no 8 pp 2855ndash2873 2011
[67] M A Quesada R Blanco-Portales S Pose et al ldquoAntisensedown-regulation of the FaPG1 gene reveals an unexpectedcentral role for polygalacturonase in strawberry fruit softeningrdquoPlant Physiology vol 150 no 2 pp 1022ndash1032 2009
[68] A Aharoni C H R De Vos M Wein et al ldquoThe straw-berry FaMYB1 transcription factor suppresses anthocyanin andflavonol accumulation in transgenic tobaccordquoThePlant Journalvol 28 no 3 pp 319ndash332 2001
[69] C A Bustamante H G Rosli M C Anon P M Civello andG A Martınez ldquo120573-Xylosidase in strawberry fruit isolation ofa full-length gene and analysis of its expression and enzymaticactivity in cultivars with contrasting firmnessrdquo Journal of PlantSciences vol 171 no 4 pp 497ndash504 2006
[70] F J Molina-Hidalgo A R Franco C Villatoro et al ldquoThestrawberry (Fragariatimesananassa) fruit-specific rhamnogalactur-onate lyase 1 (FaRGLyase1) gene encodes an enzyme involvedin the degradation of cell-wall middle lamellaerdquo Journal ofExperimental Botany vol 64 no 6 pp 1471ndash1483 2013
[71] C R Figueroa H G Rosli P M Civello G A Martınez RHerrera and M A Moya-Leon ldquoChanges in cell wall polysac-charides and cell wall degrading enzymes during ripeningof Fragaria chiloensis and Fragaria timesananassa fruitsrdquo ScientiaHorticulturae vol 124 no 4 pp 454ndash462 2010
[72] E M J Salentijn A Aharoni J G Schaart M J Boone and FA Krens ldquoDifferential gene expression analysis of strawberrycultivars that differ in fruit-firmnessrdquo Physiologia Plantarumvol 118 no 4 pp 571ndash578 2003
[73] M C Dotto G A Martınez and P M Civello ldquoExpressionof expansin genes in strawberry varieties with contrasting fruitfirmnessrdquo Plant Physiology and Biochemistry vol 44 no 5-6pp 301ndash307 2006
[74] W Schwab J G Schaart and C Rosati ldquoFunctional molecularbiology research in Fragariardquo in Genetics and Genomics ofRosaceae pp 457ndash486 Springer 2009
[75] G Cumplido Laso ldquoFunctional characterization os satrawberry(Fragaria x Ananassa) fruit-specific and ripening-related genesinvolved in aroma and anthochyanins biosynthesisrdquo PhD The-sis Universidad de Cordoba 2012
[76] G B Seymour C D Ryder V Cevik et al ldquoA SEPALLATAgene is involved in the development and ripening of strawberry(Fragariatimesananassa Duch) fruit a non-climacteric tissuerdquoJournal of Experimental Botany vol 62 no 3 pp 1179ndash11882011
12 BioMed Research International
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
[77] A Banerjee and A Roychoudhury ldquoGroup II late embryogene-sis abundant (LEA) proteins structural and functional aspectsin plant abiotic stressrdquo Plant Growth Regulation vol 79 no 1pp 1ndash17 2016
[78] D Du Q Zhang T Cheng H Pan W Yang and L SunldquoGenome-wide identification and analysis of late embryogene-sis abundant (LEA) genes in Prunus mumerdquoMolecular BiologyReports vol 40 no 2 pp 1937ndash1946 2013
[79] F Bao D Du Y An et al ldquoOverexpression of Prunus mumedehydrin genes in tobacco enhances tolerance to cold anddroughtrdquo Frontiers in Plant Science vol 8 article 151 2017
[80] R Sasaki H Yamane T Ooka et al ldquoFunctional and expres-sional analyses of PmDAM genes associated with endodor-mancy in Japanese apricot (Prunus mume)rdquo Plant Physiologyvol 157 no 1 pp 485ndash497 2011
[81] Z Li G L Reighard A G Abbott and D G BielenbergldquoDormancy-associated MADS genes from the EVG locus ofpeach [Prunus persica (L) Batsch] have distinct seasonal andphotoperiodic expression patternsrdquo Journal of ExperimentalBotany vol 60 pp 3521ndash3530 2009
[82] H Yamane T Ooka H Jotatsu R Sasaki and R Tao ldquoExpres-sion analysis of PpDAM5 and PpDAM6 during flower buddevelopment in peach (Prunus persica)rdquo Scientia Horticulturaevol 129 no 4 pp 844ndash848 2011
[83] V Gregis A Sessa L Colombo andMM Kater ldquoAGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floralmeristem identity inArabidopsisrdquoThePlant Journal vol 56 no6 pp 891ndash902 2008
[84] V Falara G A Manganaris F Ziliotto et al ldquoA 120573-D-xylosidaseand a PR-4B precursor identified as genes accounting fordifferences in peach cold storage tolerancerdquo Functional ampIntegrative Genomics vol 11 no 2 pp 357ndash368 2011
[85] E Dirlewanger J Quero-Garcıa L Le Dantec et al ldquoCompar-ison of the genetic determinism of two key phenological traitsflowering and maturity dates in three Prunus species Peachapricot and sweet cherryrdquoHeredity vol 109 no 5 pp 280ndash2922012
[86] D Ravaglia R V Espley R A Henry-Kirk et al ldquoTranscrip-tional regulation of flavonoid biosynthesis in nectarine (Prunuspersica) by a set of R2R3MYB transcription factorsrdquoBMCPlantBiology vol 13 article 68 2013
[87] T Nakano K Suzuki T Fujimura and H Shinshi ldquoGenome-wide analysis of the ERF gene family in arabidopsis and ricerdquoPlant Physiology vol 140 no 2 pp 411ndash432 2006
[88] M Gonzalez-Aguero S Troncoso O Gudenschwager RCampos-VargasM AMoya-Leon and B G Defilippi ldquoDiffer-ential expression levels of aroma-related genes during ripeningof apricot (Prunus armeniaca L)rdquo Plant Physiology and Bio-chemistry vol 47 no 5 pp 435ndash440 2009
[89] M Tatsuki N Nakajima H Fujii et al ldquoIncreased levelsof IAA are required for system 2 ethylene synthesis causingfruit softening in peach (Prunus persica L Batsch)rdquo Journal ofExperimental Botany vol 64 pp 1049ndash1059 2013
[90] Y-Q Wen F He B-Q Zhu et al ldquoFree and glycosidicallybound aroma compounds in cherry (Prunus avium L)rdquo FoodChemistry vol 152 pp 29ndash36 2014
[91] T Horibe K Yamada S Otagaki et al ldquoMolecular geneticstudies on continuous-flowering roses that do not originatefrom Rosa chinensisrdquo in Proceedings of the 6th InternationalSymposium on Rose Research and Cultivation vol 1064 pp 185ndash192 2013
[92] L-N Wang Y-F Liu Y-M Zhang R-X Fang and Q-L LiuldquoThe expression level of Rosa Terminal Flower 1 (RTFL1) isrelated with recurrent flowering in rosesrdquo Molecular BiologyReports vol 39 no 4 pp 3737ndash3746 2012
[93] H Iwata AGaston A Remay et al ldquoTheTFL1 homologueKSNis a regulator of continuous flowering in rose and strawberryrdquoThe Plant Journal vol 69 no 1 pp 116ndash125 2012
[94] S Hanano and K Goto ldquoArabidopsis TERMINAL FLOWER1 isinvolved in the regulation of flowering time and inflorescencedevelopment through transcriptional repressionrdquo The PlantCell tpc 111088641 2011
[95] M Notaguchi M Abe T Kimura et al ldquoLong-distance graft-transmissible action of Arabidopsis FLOWERING LOCUS Tprotein to promote floweringrdquo Plant and Cell Physiology vol49 pp 1645ndash1658 2008
[96] S Otagaki Y Ogawa L Hibrand-Saint Oyant et al ldquoGenotypeof FLOWERING LOCUS T homologue contributes to flower-ing time differences in wild and cultivated rosesrdquoThe Journal ofPlant Biology vol 17 no 4 pp 808ndash815 2015
[97] D P Wickland and Y Hanzawa ldquoThe FLOWERING LOCUSTTERMINAL FLOWER 1 gene family functional evolutionand molecular mechanismsrdquo Molecular Plant vol 8 no 7 pp983ndash997 2015
[98] I Guterman M Shalit N Menda et al ldquoRose scent genomicsapproach to discovering novel floral fragrancendashrelated genesrdquoThe Plant Cell vol 14 pp 2325ndash2338 2002
[99] Y Kaminaga J Schnepp G Peel et al ldquoPlant phenylacetalde-hyde synthase is a bifunctional homotetrameric enzyme thatcatalyzes phenylalanine decarboxylation and oxidationrdquo TheJournal of Biological Chemistry vol 281 no 33 pp 23357ndash233662006
[100] A Joichi K Yomogida K-I Awano and Y Ueda ldquoVolatilecomponents of tea-scented modern roses and ancient Chineserosesrdquo Flavour and Fragrance Journal vol 20 no 2 pp 152ndash1572005
[101] I Flament C Debonneville and A Furrer ldquoVolatile com-pounds of roses characterization of cultivars based on theheadspace analysis of living flower emissionsrdquo ACS SymposiumSeries 1993
[102] G Scalliet N Journot F Jullien et al ldquoBiosynthesis ofthe major scent components 35-dimethoxytoluene and 135-trimethoxybenzene by novel rose O-methyltransferasesrdquo FEBSLetters vol 523 no 1-3 pp 113ndash118 2002
[103] D Tholl and J Gershenzon ldquoThe flowering of a new scentpathway in roserdquo Science vol 349 no 6243 pp 28-29 2015
