Transitioning to the Next Phase: The Role of SugarSignaling throughout the Plant Life Cycle[OPEN]
Astrid Wingler1
School of Biological, Earth and Environmental Sciences, University College Cork, T23 TK30, Cork, Ireland
ORCID ID: 0000-0003-4229-2497 (A.W.).
Developmental transitions in plants require adequatecarbon supply, which can be sensed through sugarsignaling. Plants have sugar signaling pathways forhigh carbon availability (including hexokinase-1 [HXK1],trehalose-6-P [T6P], and target of rapamycin [TOR]) andfor starvation (including Snf1-related protein kinase-1 [SnRK1] and C/S1 bZIP transcription factors) with in-teractions between them. If new sinks are created, forexample, during floral transition, high carbon signals arerequired to progress to the next phase in develop-ment while low carbon signals can delay such tran-sitions. Other developmental processes, for example,seed development, require high and low carbonsignals. Recent findings suggest that sugar signalingpathways interact with developmental regulation bymicroRNA156 (miR156). For example, T6P interactswith miR156 during the floral transition, but interac-tions between T6P and miR156 during other develop-mental transitions have not been described. ThisUpdatecompares the role of sugar signaling pathways through-out the plant life cycle (seed germination, cotyledongreening, juvenile-to-adult phase transition, floral transi-tion, shoot branching, senescence, and seeddevelopment)to identify common and distinct components and theirinteractions in the context of source-sink relationships.
Developmental transitions in plants result in changesin the source-sink relationship. For example, the growthof new organs can create additional carbon sinks andtherefore requires a minimum availability of carbonreserves. If carbon availability is insufficient, there is arisk of premature carbon depletion, resulting, for ex-ample, in seedling death, or abortion of fruit or seeddevelopment. Sugar signals can regulate developmen-tal transitions and thereby signal if sufficient carbon isavailable for successful completion of a developmentalprogram. However, the response to sugars and in-volvement of individual signaling pathways may varythroughout the plant life cycle as sugar signals interactwith other developmental and environmental factors.
This Update analyzes older and recent findings toidentify common and distinct sugar signaling pathways
across developmental transitions in the context ofchanges in the source-sink relationship. Excellent re-views on the role of sugar signaling in plant develop-ment have been published in recent years. Most of thesefocus on specific signaling pathways or developmentalprocesses, for example, on flowering and interactionwith hormones (Matsoukas, 2014a), growth (Lastdrageret al., 2014), T6P (O’Hara et al., 2013), T6P and SnRK1(Tsai and Gazzarrini, 2014), hexokinase (Granot et al.,2014), miRNAs (Yu et al., 2015), or SnRK1 and TOR(Baena-González and Hanson, 2017). The whole life cy-cle of the plant is considered here (Box 1), including stepchanges (such as floral transition) as well as moregradual processes (such as leaf senescence). Because ofspace limitations, sugar signaling in root development(Thompson et al., 2017) is not specifically covered.Whilethis Update focuses on sugars as signals for carbonavailability, it should be kept in mind that sugar signalsalso interact with nitrogen (e.g. Osuna et al., 2015; Whiteet al., 2016) and hormone (e.g. Matsoukas, 2014a) sig-naling pathways.
1 Address correspondence to [email protected]. wrote the article.[OPEN] Articles can be viewed without a subscription.www.plantphysiol.org/cgi/doi/10.1104/pp.17.01229
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SUGAR SIGNALING PATHWAYS FOR HIGH ANDLOW CARBON AVAILABILITY
In plants, Suc is the predominant sugar formed byphotosynthesis, while hexoses (Glc and Fru) are mainlybreakdown products of Suc and starch. The main plantsugar signaling pathways considered in this Update arelisted in Box 2.
Hexose accumulation in response to high carbonavailability results in the down-regulation of photo-synthetic gene expression. This prevents overinvest-ment of nitrogen in the photosynthetic apparatus.Hexose accumulation in plants can be sensed by HXK1(Granot et al., 2014). Importantly, it was shown thatcatalytically inactive HXK1 mutant forms still have asignaling function, supporting the view that the role ofHKX1 in signaling high sugar availability is indepen-dent of its role in Glc metabolism (Moore et al., 2003).More recent work has shown that HXK1 also mediatesstomatal closure, thereby contributing to the feedbackeffect of sugar accumulation on photosynthesis (Kellyet al., 2012; Kelly et al., 2013).
Only low amounts of the disaccharide trehalose arepresent in plants (Wingler, 2002). Nevertheless, T6P, theprecursor of trehalose in the biosynthetic pathway, hasbeen identified as an important signaling molecule in
plants (O’Hara et al., 2013). T6P is synthesized fromUDP-Glc and Glc-6-P by T6P synthase (TPS) and hy-drolyzed to trehalose by T6P phosphatase (TPP). It ac-cumulates under conditions when Suc content is highand has been proposed to act as a signal for Suc avail-ability (Nunes et al., 2013a; Yadav et al., 2014; Figueroaand Lunn, 2016). The role of T6P in regulating source-sink interactions during plant development is furtherdiscussed by O’Hara et al. (2013) and Griffiths et al.(2016a).
In addition to T6P, the protein kinase TOR signals highcarbon availability and stimulates protein translation andplant growth (Deprost et al., 2007; Lastdrager et al., 2014).Despite their common function in promoting growthin response to carbon availability, no direct interactionbetween T6P and TOR signaling has been identified(Figueroa and Lunn, 2016), which supports the view thatT6P is mainly involved in Suc signaling, whereas TORmay be responsible for Glc signaling (Dobrenel et al.,2016), although independently of the HXK1-dependentGlc signaling pathway (Xiong et al., 2013).
In contrast to the growth-stimulating activity ofTOR, SnRK1 inhibits growth at low carbon supply(Lastdrager et al., 2014) and is generally consideredto be responsible for signaling low energy availability(Baena-González et al., 2007; Baena-González andSheen, 2008). The regulation of SnRK1 is complex, in-cluding AMP-dependent regulation of its phosphoryl-ation and other posttranslational modifications (Crozetet al., 2014), in addition to direct inhibition by T6P andother sugar phosphates (Zhang et al., 2009; Nunes et al.,2013b). T6P inhibits the catalytic activity of SnRK1in vitro and in vivo (Zhang et al., 2009). However, in-hibition of SnRK1 by T6P requires a protein factor thatis not present in mature tissues, and the interactionbetween SnRK1 and T6P is unlikely to be solely re-sponsible for T6P effects (Figueroa and Lunn, 2016).SnRK1 acts at least partially via activation of the C/S1group of bZIP transcription factors (Baena-Gonzálezet al., 2007). Recently, a mechanism for this activation
has been described: By phosphorylation of the C-groupbZIP63, SnRK1 promotes bZIP homo- and hetero-dimerization, for example, with S-group bZIPs (such asbZIP11) that are not themselves phosphorylated bySnRK1 (Mair et al., 2015). Similar to SnRK1, C/S1 groupbZIP transcription factors, whose expression is controlledby Suc-induced repression of translation (Weltmeieret al., 2009), are involved in reprogramming metabolismin response to low energy supply.Sugar signaling interacts with miRNAs in regulating
development, specifically miR156 (Matsoukas, 2014b;Yu et al., 2015). High sugar availability results in thedown-regulation of miR156 expression and, as a result,increased expression of its targets, the Squamosa Pro-moter Binding Protein-Like (SBP/SPL) transcriptionfactor genes (Fig. 1). SPL expression, in turn, increasesexpression of miR172, which leads to the activation of,for example, flowering (Matsoukas, 2014b; Yu et al.,2015; Hyun et al., 2017).
GERMINATION AND COTYLEDON GREENING
Seed reserves are important for seedling establish-ment, but high external sugar supply (e.g. 6% Glc) in-hibits seedling germination and cotyledon greening,resulting in developmental arrest. Mutants in the plastid
Glc-6-P/P translocator (GPT2) showed decreased sensi-tivity to Glc during germination, whereas sensitivityto Glc during cotyledon greening was increased andseedling establishment delayed (Dyson et al., 2014).These results demonstrate that sugar transport across theplastid membrane modulates the sugar response, andalso that germination and cotyledon greening are notalways regulated by the same pathways.
Developmental arrest of seedling development inresponse to high sugar supply was used for the isola-tion of Glc and Suc insensitive mutants (for review, seeGibson, 2004; Osuna et al., 2015). Abscisic acid (ABA)insensitive (abi) and ABA deficient (aba) mutants havebeen shown to be insensitive to highGlc concentrations,demonstrating an overlap between ABA and sugarsignaling, but sugar signals also interact with ethylene,gibberellin, cytokinin, and auxin (Gibson, 2004). In theabsence of nitrogen and other inorganic nutrients, alower concentration of 2% Glc also results in develop-mental arrest, although in this case without involvementof ABA signaling (Cho et al., 2010). Another Glc-insensitive mutant (gin2-1) harbors a mutation in thegene for the sugar sensor HXK1 (Moore et al., 2003). Inthe absence of inorganic nutrients, this mutant alsoshows insensitivity to a low concentration of 2%Glc andcan be complemented with catalytically inactive mutantversions of HXK1 (Cho et al., 2010). Similar to the hxk1mutation, overexpression of hexokinase-like1 (HKL1)reduces seedling sensitivity to high Glc concentration,suggesting an antagonistic function of HXK1 and HKL1with respect to seedling development (Karve andMoore,2009; Karve et al., 2012).
T6P interacts with ABA during seedling develop-ment. Overexpression of the Arabidopsis (Arabidopsisthaliana) TPS gene TPS1 results in reduced Glc andABAsensitivity, and in contrast to wild-type plants, TPS1-overexpressing seedlings do not accumulate ABA inresponse to Glc treatment (Avonce et al., 2004). Mutantswith weak TPS1 alleles, on the other hand, are hyper-sensitive to ABA during germination (Gómez et al.,2010). TOR expression also decreases sugar and ABAsensitivity (Deprost et al., 2007), indicating that pathwaysfor high sugar availability increase sugar utilization forgrowth and thereby prevent feedback inhibition of pho-tosynthetic development.
In addition, SnRK1 has been implicated in seed ger-mination and seedling growth in interaction with ABAsignaling. In Arabidopsis, overexpression of the SnRK1gene AKIN10 results in delayed germination (Tsai andGazzarrini, 2012) and hypersensitivity to Glc and ABAduring seedlingdevelopment (Jossier et al., 2009). SnRK1acts by phosphorylating and stabilizing FUSCA3 (FUS3;Tsai and Gazzarrini, 2012); FUS3 promotes ABA syn-thesis, while ABA, in turn, stimulates SnRK1 (Tsai andGazzarrini, 2014). Overall this leads to ABA-dependentinhibition of seed germination.
While most forms of stress (e.g. drought, cold, salt)lead to sugar accumulation in plants, hypoxia undersubmergence results in starvation. Anaerobic germi-nation requires mobilization of starch and fueling of
Figure 1. Model for the role of sugar signaling during the juvenile-to-adult phase transition and floral transition, combining elements of themodels presented by Tsai and Gazzarrini (2014) and Yu et al. (2015), inaddition to highlighting the function of T6P in leaves and the shootapical meristem (SAM), and the potential functions of HXK1 and TOR.T6Pand SnRK1may play a role in the juvenile-to-adult phase transition,in addition to flowering, but their role in this transition is not well un-derstood. Red components are involved in high carbon signaling, bluecomponents in starvation signaling.
fermentation by glycolysis. A rice (Oryza sativa) TPPgene (TPP7) was identified as QTL for anaerobic ger-mination tolerance (Kretzschmar et al., 2015). Presenceof a functional TPP results in a lower T6P/Suc ratio andincreased amylase-dependent starch mobilization forcoleoptile growth. These findings, together with thefunction of SnRK1 for germination under starvation (Luet al., 2007), are consistent with starvation signals beingrequired for starch mobilization during anaerobic ger-mination and an antagonistic function of T6P andSnRK1. Coleoptile length during germination at lowoxygen was decreased in rice hexokinase (HXK7) mu-tants but increased in overexpressors (Kim et al., 2016).The authors suggest that HXK7 fuels anaerobic fer-mentation and that its catalytic function rather than itsrole in sugar signaling is responsible for anaerobicgermination tolerance.
JUVENILE-TO-ADULT PHASE TRANSITION
The juvenile-to-adult phase transition comprisesmajor morphological changes during shoot develop-ment (heteroblasty or vegetative phase change) as wellas developmental changes that result in the competenceto flower under inductive conditions (Poethig, 2010). Insome woody species (e.g. Hedera helix, some Acacia andEucalyptus species), juvenile leaves have a differentmorphology compared with adult leaves, and somefruit trees (e.g. apple) need to reach a certain age to gainthe competence to flower (Poethig, 2013). In the Bras-sicaceae, the juvenile-to-adult phase transition en-hances the flowering response to inductive long days(Matsoukas et al., 2013) or vernalization (Bergonzi et al.,2013; Zhou et al., 2013).
The relationship between heteroblasty and attain-ment of floral competence differs between species, andsome species may even flower before vegetativechanges become apparent (Poethig, 2010). Differentsignaling pathways may therefore exist (Matsoukas,2014b; Hyun et al., 2017). Nevertheless, the juvenile-to-adult phase transition and attainment of floral compe-tence are both controlled by decreased expression ofmiR156 and increased expression of its targets, thegroup of SBP/SPL transcription factor genes (Wu andPoethig, 2006; Wu et al., 2009; Xu et al., 2016; Fig. 1).
The juvenile-to-adult phase transition is dependenton shoot-derived factors associated with photosynthe-sis (Poethig, 2013). A role of sugar supply in the heter-oblastic transition was demonstrated in research withthe waterfern Marsilea (Allsopp, 1954): Addition ofsugar to the culture medium resulted in earlier forma-tion of adult leaves, and this process could be reversedby transfer to a sugar-free medium. In Arabidopsis,vegetative phase change from juvenile to adult leaves ischaracterized by increased leaf complexity, includingthe formation of abaxial trichomes and serrated mar-gins. This transition is delayed in defoliated plants andin photosynthetic mutants (Yang et al., 2013; Yu et al.,2013; Buendía-Monreal and Gillmor, 2017), supporting
the view that sugar produced in photosynthesis is in-volved. Under low sugar availability, high miR156abundance prevents the transition from juvenile toadult leaves, whereas sugar supply represses the tran-scription of MIR156 genes and promotes phase change(Yang et al., 2013; Yu et al., 2013). Yu et al. (2013) showthat this regulatory effect is evolutionarily conserved asSuc supply does not only repress miR156 in Arabi-dopsis, but also in other flowering plants and in themoss Physcomitrella patens.
There is also evidence for an involvement of HXK1-dependent signaling in the transition, however notnecessarily in the way that would be expected. If HXK1were responsible for the sensing of Glc during thejuvenile-to-adult phase transition, one would expectthe HXK1 mutant gin2-1 to have an extended juvenilephase as it cannot respond to hexose accumulation.However, Yang et al. (2013) showed that gin2-1 pro-duces fewer juvenile leaves and has lower levels ofmiR156 than wild-type plants, consistent with acceler-ated phase transition, although the differences were notvery large. Matsoukas et al. (2013) determined thelength of the juvenile phase as insensitivity to floweringinduction upon transfer to long days and also observedthat gin mutants, including gin2-1, had a shorter juve-nile phase. The observation that mutants in starchsynthesis as well as mutants in starch breakdown showan extended juvenile phase length demonstrates thecomplexity of carbohydrate signaling (Matsoukas et al.,2013). Sincemutants in starch synthesis and breakdownhave lower nighttime Suc contents than wild-typeplants, starvation during the night may be responsiblefor the delay in the juvenile-to-adult phase transition,but what the exact signal is and how it is sensed are notentirely clear.
A model for the potential involvement of SnRK1 andT6P in the juvenile-to-adult phase transition and flow-ering was developed by Tsai and Gazzarrini (2014). Itwas shown that T6P interacts with miR156 signalingduring the floral transition (see below), but how SnRK1and T6P may interact with miR156 in the vegetative(heteroblastic) transition remains an open question.
FLORAL TRANSITION
Under inductive conditions, the juvenile-to-adultphase transition is followed by the floral transition(vegetative-to-reproductive phase transition). It is notalways possible to differentiate the processes duringwhich plants acquire the competence to flower as partof the juvenile-to-adult phase transition from those re-sponsible in floral transition as such, and the mainfunction of sugars may be in regulating the competenceto flower (Hyun et al., 2017). Accordingly, the regula-tory framework of the juvenile-to-adult phase transi-tion and floral transition appears to be the same (Fig. 1),with miR156-dependent repression of SPL genes andincreased miR172 expression also involved in the reg-ulation of flowering (Matsoukas, 2014b; Yu et al., 2015).
While there is overlap in SPL function, different mem-bers of the SPL transcription factor family also havespecific developmental functions in vegetative phasechange and the floral transition (Xu et al., 2016).Sugar availability is an important signal in floral in-
duction. For example, it was observed that Suc con-centration in leaf exudate increases in response to aninductive long day (Corbesier et al., 1998), and Sucsupply can promote flowering of Arabidopsis plantseven in the dark (Roldán et al., 1999). It was thereforediscussed if Suc may act as florigen (Corbesier andCoupland, 2006). While Flowering Locus T (FT) proteinhas since been identified as a long-distance signal forfloral induction (Corbesier et al., 2007), this does notexclude the possibility that additional florigens, such asgibberellins and Suc, play an important role in modu-lating flowering time (King, 2012), e.g. via stimulatingFT expression (King et al., 2008).Work with transgenic plants has supported the view
that flowering is regulated by sugar metabolism. Plantsoverexpressing the Suc biosynthetic enzyme Suc-P syn-thase flowered earlier and produced more flowers(Micallef et al., 1995; Baxter et al., 2003). Meristem-specific expression of the Suc-hydrolyzing enzyme cellwall invertase also led to accelerated flowering and in-creased seed yield, whereas expression of cytosolic in-vertase had the opposite effect (Heyer et al., 2004).Mutants in starch synthesis and breakdown flower late(Corbesier et al., 1998), in addition to having an extendedjuvenile phase (Matsoukas et al., 2013). These findingssupport a role for Suc or the Suc/hexose ratio in flow-ering regulation. However, the response to Suc is notstraightforward, as demonstrated by a delay offloweringat high (5%) external Suc concentration (Ohto et al., 2001).Several lines of evidence support the view that T6P is
required as a sugar signal in the regulation of flowering:Plants with lower T6P through expression of the Esch-erichia coli TPP or TPH (trehalose-6-P hydrolase) genesfor T6P breakdown flower late (Schluepmann et al.,2003). Mutants in the Arabidopsis TPS gene (tps1 mu-tants) are embryo lethal, but they can be rescued byexpression of TPS1 from a dexamethasone induciblepromoter (van Dijken et al., 2004) or a seed-specificpromoter (Gómez et al., 2010) to investigate the effectof a lack of TPS1 expression after germination. In bothcases, growth was strongly reduced and no floweringoccurred in the absence of TPS1 expression, while lowTPS1 expression after dexamethasone treatment or inplants with weak TPS1 alleles resulted in delayedflowering comparedwithwild-type plants. More recentwork shed light on how T6P regulates flowering. Re-pression of TPS1 through the use of artificial miRNAshowed that T6P synthesis is required for the expres-sion of FT (Wahl et al., 2013). In the shoot apical meri-stem, T6P is involved in the down-regulation of miR156expression, which is required for flowering, whereas inthe leaves T6P acts directly by regulating FT expression(Fig. 1). In addition to the role of T6P in floral transition,a function of TOR in promoting flowering has beensuggested (Ren et al., 2012).
Overexpression of the SnRK1 gene AKIN10 leads todelayed flowering (Baena-González et al., 2007; Tsaiand Gazzarrini, 2012). SnRK1 phosphorylates the In-determinate Domain (IDD) transcription factor IDD8,which results in its inactivation and delayed floweringunder sugar starvation (Jeong et al., 2015).While SnRK1and IDD8 have opposite functions in the regulationof flowering in response to carbon availability, over-lapping functions between SnRK1 and its target FUS3(which is stabilized after phosphorylation by SnRK1)have been described (Tsai and Gazzarrini, 2012). Thefindings discussed here are consistent with signalingpathways for high carbon availability inducing andSnRK1 repressing the floral transition.
SHOOT BRANCHING
Shoot branching results from the release of axillarybud dormancy. The classical view is that shootbranching is inhibited by auxin transport from theshoot apex to axillary buds (resulting in apical domi-nance) and that auxin depletion upon removal of theshoot tip is responsible for increased shoot branching.However, Mason et al. (2014) proposed that auxin de-pletion is not sufficient to trigger bud release. Instead,they show that, upon removal of pea (Pisum sativum)shoot tips, more Suc is transported to the axillary buds,where it reduces expression of the branching inhibitorBranched1 gene. This effect is dependent on the presenceof source leaves, supporting the notion that sink-sourcerelationships determine shoot branching (Mason et al.,2014).
Meristem-specific overexpression of cell wall or cy-tosolic invertase in Arabidopsis changes the shootbranching pattern in a complex manner, differentiallyaffecting the formation of axillary inflorescences,branching of the main inflorescence, and branching ofside inflorescences (Heyer et al., 2004). This suggeststhat the Suc/hexose ratio in specific cellular compart-ments is critical for the branching pattern.
The Suc signal may be mediated by T6P signaling(Barbier et al., 2015). Apical dominance is enhanced inplants with lower T6P due to expression of the E. coli TPPor TPH genes, whereas plants expressing the E. coli TPSgene show increased branching, suggesting a role of T6Pas a sugar signal in branching control (Schluepmann et al.,2003; van Dijken et al., 2004). The observation that themaize (Zea mays) Ramosa3 gene, which regulates tasseland ear branching, encodes a TPP enzyme supports afunction of T6P in inflorescence branching (Satoh-Nagasawa et al., 2006). A similar role was recently sug-gested for the grape (Vitis vinifera) Sister of Ramosa3(VvSRA; Ishiai et al., 2016), although a direct involvementin T6P breakdown was not demonstrated. Eveland andJackson (2012) point out that themaizeRamosa3may alsoact as a transcriptional regulator and that its functionmaytherefore not solely depend on its TPP catalytic activity.
In addition to T6P, HXK1 is involved in increasedbranching, as suggested by a loss of apical dominance
in transgenic HXK1-overexpressing Arabidopsis plants(Kelly et al., 2012). Mutations in genes encoding pro-teins that interact with TOR also suggest a function ofTOR-dependent signaling in the regulation of apicaldominance and shoot branching: Mutants in Raptor(Anderson et al., 2005) or LST8 (Moreau et al., 2012)have increased shoot branching, suggesting that theTOR pathway may inhibit shoot branching, althoughhow this may affect the response to sugar availabilityhas not been investigated.
Overall, there is strong evidence for a key role of sugarsin the branching of vegetative shoots and inflorescences,but to what extent they are simply fueling growth, act asmetabolic regulators, or interact with other developmen-tal pathways is not always clear. In addition, miR156overexpression enhances shoot branching in Arabidopsis(Schwarz et al., 2008; Wei et al., 2012) and Brachypodiumdistachyon (An et al., 2015). Whether this regulation is re-lated to sugar signaling is, however, unknown.
SENESCENCE
During leaf senescence, nutrients are recycled from theold leaves. For example, nitrogen from photosyntheticproteins is exported and can be invested in the photo-synthetic apparatus of younger organs or stored in seedstorage proteins. Photosynthesis declines during thisprocess, but in the absence of strong sinks, old leaves donot become carbon starved and sugars can accumulate(Wingler et al., 2006). Senescence can be induced by darktreatment, which results in starvation, but global changesin gene expression during dark treatment only show littlesimilarity with developmental senescence (Wingler et al.,2009). Instead, senescence triggered by a combination oflow nitrogen with 2% Glc supply (Wingler et al., 2004;Pourtau et al., 2004, 2006) shows high similarity withdevelopmental senescence (Wingler and Roitsch, 2008;Wingler et al., 2009). Sugar accumulation in old leavessignals an excess of carbon relative to nitrogen availabil-ity, and sugars can thereby integrate other environmentalsignals to regulate nitrogen allocation (Wingler et al.,2006). Glc treatment only induces senescence from a cer-tain stage of development onwards (Wingler et al., 2012).This is in agreement with gene expression studies show-ing that sugar accumulation predominantly repressesphotosynthetic genes in older plants (unpublished com-parison of microarray data by Price et al. [2004], Lloydand Zakhleniuk [2004], and Pourtau et al. [2006]). A de-velopmental time window for senescence regulation wasproposed by Jing et al. (2002), who show that senescencecan only be induced by ethylene during a defined period,suggesting that developmental factors are required togain the competence to senesce.
Feeding of themetabolizable sugars Glc, Fru, and Sucinduces senescence to a similar extent (Wingler et al.,2012). However, a function of cell wall invertase activ-ity in delaying leaf senescence in tobacco (Nicotianatabacum; Lara et al., 2004) and tomato (Solanum lyco-persicum; Jin et al., 2009) suggests that the Suc/hexose
ratio in the apoplast is responsible, probably by influ-encing sink activity in the old leaves. Within the cells,HXK1-dependent signaling is involved in senescenceregulation. Transgenic tomato (Dai et al., 1999;Swartzberg et al., 2011) and Arabidopsis (Kelly et al.,2012) plants overexpressing the Arabidopsis HXK1have accelerated senescence, whereas theHXK1mutantgin2-1 shows delayed senescence (Moore et al., 2003)and a reduced senescence response to Glc treatment(Pourtau et al., 2006). While these findings support arole of HXK1 signaling in senescence regulation, a lackof HXK1 does not completely abolish the effect of sugartreatment on senescence, suggesting that other signal-ing pathways are involved.
In addition to HXK1, T6P is involved in senescenceregulation in response to sugar availability. T6P accu-mulates during senescence in parallel with an increase insugar contents (Wingler et al., 2012), and transgenic plantsexpressing a bacterial TPP gene to lower T6P content ex-hibit delayed senescence, as indicated by delayed leafyellowing, decreased expression of senescence-associatedgenes, and a lack of anthocyanin accumulation (Wingleret al., 2012). In addition, these plants do not show thetypical senescence response to sugar treatment, suggest-ing that T6P is required for the induction of senescence bysugar availability. Transfer between different media withand without sugar showed that T6P only acts during acertain time window, after which sugar treatment alsoinduces senescence in plants with low T6P (Wingler et al.,2012). This indicates that senescence induction at a laterdevelopmental stage is no longer T6P dependent. SnRK1delays senescence (Baena González et al., 2007; Tsai andGazzarrini, 2012), which is consistent with inhibition ofSnRK1 by T6P (Zhang et al., 2009). However, inhibition ofSnRK1 by T6P requires an additional factor that is presentin growing tissues but not in senescing leaves (Wingleret al., 2012). If T6P acts via SnRK1, it would therefore haveto initiate senescence before the symptoms become visi-ble, which is supported by the notion that T6P is requiredfor early developmental changes that result in the com-petence to respond to other senescence-inducing factors,such as Glc or ethylene.
Inhibition of TOR delays senescence and flowering,which supports the notion that high energy availabilitypromotes senescence (Ren et al., 2012). Since the timingof flowering and senescence is related (Wingler et al.,2010; Wingler, 2011), accelerated developmental se-nescence in response to high carbon availability may bea consequence of earlier flowering.
SEED DEVELOPMENT
During embryo maturation, storage compounds aresynthesized in preparation for desiccation and dor-mancy. This stage is therefore characterized by a strongsink activity, and carbon signaling processes that reg-ulate this process have been well researched. Embryodevelopment in mutants in the Arabidopsis TPS (tps1mutants) is arrested at the torpedo stage, showing that
T6P is required for embryo maturation, especially forcell division and cell wall synthesis (Eastmond et al.,2002; Gómez et al., 2006). Using an elegant chemicalapproach, it was recently shown that T6P can directlypromote grain filling in wheat (Triticum aestivum).Spraying of wheat plants with compounds that releaseT6P upon exposure to sunlight led to increased grainyield due to the formation of larger grains with higherstarch content (Griffiths et al., 2016b). Earlier work hadshown that T6P naturally accumulates in wheat grainsto previously unreported levels before grain filling(Martínez-Barajas et al., 2011). Interestingly, T6P contentwas low in the embryonic and maternal tissues and ac-cumulated almost exclusively in the endosperm, althoughat later stages it may also be required in the embryo itself.In addition to T6P, TOR is required for endosperm andembryo development (Menand et al., 2002).SnRK1 plays an important role in pea seed develop-
ment: Antisense repression of SnRK1 in seeds resultedin defects in seed maturation and storage protein syn-thesis via ABA synthesis and/or signaling (Radchuket al., 2006, 2010). SnRK1 has been proposed to regulateseedmaturation by interactingwith FUS3 and hormonesignaling pathways (Tsai and Gazzarrini, 2012).SnRK1-dependent phosphorylation stabilizes FUS3,which is required for maturation by positively regu-lating ABA synthesis (Tsai and Gazzarrini, 2012, 2014).SnRK1 thus has a positive effect on seedmaturation andstorage protein synthesis, which is opposite to itscharacteristic role in starvation signaling and activationof catabolic pathways (Baena-González and Sheen,2008). In developing wheat grains, in vitro SnRK1 ac-tivity was reported in the embryo and endosperm,which together with low T6P in the embryo may sup-port high in vivo SnRK1 activity for embryomaturation(Martínez-Barajas et al., 2011). The C/S1 bZIP tran-scription factors, in particular, bZIP53, which isexpressed late during seed development, have alsobeen proposed to be involved in storage protein syn-thesis and seed maturation (Weltmeier et al., 2009;Alonso et al., 2009; Restovic et al., 2017).
Signaling pathways associated with high carbonavailability (T6P and TOR) as well as those associatedwith starvation (SnRK1, C/S1-group bZIPs) are thusrequired for seed development. This may reflect dif-ferent requirements in different tissues that act assource or sink (i.e. T6P in the endosperm and SnRK1 inthe embryo), or different temporal patterns (T6P accu-mulating pregrain filling and bZIP53 being expressedduring maturation), but how exactly the various sig-naling pathways are coordinated is a question for fu-ture research.
CONCLUDING REMARKS
Developmental transitions that are associated withthe creation of new sinks are usually triggered by highcarbon signaling pathways, including T6P, hexokinase,and TOR signaling, supporting the view that thesetransitions can only go ahead when sufficient carbon isavailable (Table I). While the involvement of sugarsignaling pathways in seed germination, flowering,and senescence is well investigated, more questionsremain concerning the juvenile-to-adult phase transi-tion, shoot branching, and seed development (“Out-standing Questions”). Although the function of miR156in the juvenile-to-adult phase transition has been ex-plored in detail, interactions with sugar signaling arenot always clear. For example, the function of T6P andSnRK1 in heteroblastic transitions still needs to be in-vestigated, while information on the role of C/S1 bZIPsin developmental transitions is generally scant. Fortransitions that require complex changes in differenttissues and cells of an organ (e.g. seed development orbranching), it is necessary to investigate signaling pro-cesses at high temporal and spatial resolution, for ex-ample, using biosensors (Jones et la., 2013) or singlecell analysis of metabolites, transcripts, and proteinafter laser microdissection (Misra et al., 2014). Giventhat developmental transitions are often linked, develop-mental changes triggered by sugars early in developmentmay have later consequences (e.g. the juvenile-to-adult
Table I. Involvement of main components of sugar signaling in developmental transitions
Plus signs (+) indicate acceleration of the process by the signaling component, minus signs (2) delay. Empty cells indicate lack of information,question marks (?) that there is no strong support for an effect.
Developmental
Transition
Source/Sink
DevelopmentEffect of Sugars HXK1 T6P TOR SnRK1 C/S1 bZIP miR156
phase transition affecting floral transition, floweringaffecting senescence, and shoot branching affectingsenescence or vice versa), making it difficult to iden-tify which process specifically is regulated by a sig-naling pathway. To elucidate these relationshipsrequires developmentally timed manipulation ofsugar signaling pathways, for example, using induciblepromoters.Received August 31, 2017; accepted September 26, 2017; published September28, 2017.
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