journa l h om epa ge: www.elsev ier .com/ locate / indcrop
eview
ultivation of Iranian seedless barberry (Berberis integerrimaBidaneh’): A medicinal shrub
li Alemardana,∗, Wahab Asadib, Mehdi Rezaeic, Leila Tabrizi a, Siavash Mohammadia
Department of Horticultural Sciences, Faculty of Agricultural Sciences and Engineering, College of Agriculture and Natural Resources, University of Tehran,1587-77871 Karaj, IranDepartment of Horticultural Sciences, Faculty of Agriculture, University of Zanjan, Zanjan, IranHorticulture Department, Agriculture collage, Shahrood University, Shahrood, Iran
r t i c l e i n f o
rticle history:eceived 2 April 2013eceived in revised form 19 July 2013ccepted 23 July 2013
eywords:erberis vulgaris var. aspermaruit set
a b s t r a c t
Iranian seedless barberry or zereshk (Berberis integerrima ‘Bidaneh’, Berberidaceae) has long been culti-vated for its fruit in South Khorasan, Iran. There are more than 11,000 ha under production producingmore than 9200 tonnes of dried fruit, annually. All orchards are established from sucker propagation butgraftage should be possible. Barberry is cold hardy and drought tolerant. However, water deficits duringfruit set, growth, and maturation cause yield reduction. Shrubs should be planted 2 m × 3 m apart. Thosetrained to multiple-trunk system facilitate harvest. Biennial bearing is a problem and sometimes no fruitis harvested in the off year. The small fruits are harvested in the autumn and sun drying is a satisfactory
arthenocarpyelf-sterilityiennial bearing
system. Barberry plant and its fruit have been used in traditional medicine. They are well documented fortheir anti-diabetic, anti-cancer, and antimicrobial activities with berberine as the main active constituent.The shrub has also ornamental uses in the landscape and the fruit is used as food additive. In addition,anthocyanin of the fruit is useful as a natural coloring agent in food industries. However, Berberis speciesare alternate hosts for rust fungi (Puccinia spp.) and must be avoided in wheat growing areas. For thisreason, they have been outlawed in some countries.
Different types of barberry are famous around the world for sev-ral benefits such as medicinal, ornamental and food uses. Iranianeedless zereshk1 (Berberis integerrima ‘Bidaneh’) is commerciallyultivated for its fruit in Iran, especially in South Khorasan province.urrently, there are over 11,000 ha of cultivated seedless zereshkroducing more than 9200 tonnes of dried fruit per year (Radmehr,010). Iranian seedless barberry is drought tolerant, making it suit-ble for South Khorasan province with a dry climate and frequentater shortages. For this reason, compared to cultivation of many
ther agricultural crops, cultivation of this crop has higher eco-omic benefits for the inhabitants and, thus, thousands of theeople rely, either directly or indirectly, on Iranian seedless bar-erry. The dried fruit is used mainly as food additive in Iranianishes and the fresh fruit is used for the production of jellies, syrups,
ams, sauces, juices, fruit concentrates and carbonated beverages.n addition, anthocyanin of the fruit has recently been given muchttention and is considered as a useful additive (i.e. as a naturaloloring agent) in food industries. Moreover, it is well documentedhat the fruit and plant display medicinal properties. In the presenteview article, we provide detailed information on the cultivationnd utilization of Iranian seedless barberry.
. Biology and taxonomy
Taxonomically, the genus, Berberis, is very difficult and com-lex. Climatic and geographical variability, polyploidy, interspecificrosses, spontaneous mutations and subsequent recombinations,nd ontogenetic variations make difficulties in proper distinc-ion of the species, thus causing an intricate synonymy (Kim andansen, 1994; Landrum, 1999; Heidary et al., 2009; Rezaei et al.,011; Sodagar et al., 2012; Heidary, Unpublished). Berberis is theichest genus of barberry family (Berberidaceae) with approxi-ately 450–500 species (Ahrendt, 1961; Loconte, 1993; Kafi et al.,
002; Simpson, 2006); however, many of them may be synonymsLandrum, 1999).
Berberis members are mostly diploid (2n = 2x = 28) (Minore andudolf, 2008; Schlegel, 2010; Rounsaville and Ranney, 2010), but
few show tetraploidy (Bottini et al., 1999, 2000; Rezaei et al.,011; Sodagar et al., 2012). Bottini et al. (1999, 2000) reportedhat tetraploid barberries are grown where the precipitation isow, while diploids are limited to regions with high precipitation.imilarly, in Khorasan provinces with dry and semi dry climates,ll studied wild barberries have been tetraploids (Sodagar et al.,012; Heidary, Unpublished). Accordingly, tetraploidy seems to ben advantage against drought condition in Berberis.
Iranian barberries are divided, based on their botany, intove wild species corresponding to Berberis vulgaris L., Berberis
rthobotrys Bienert ex Schneid, Berberis crataegina DC., Berberisntegerrima Bunge and Berberis khorasanica Browicz and ZielinskiBrowicz and Zielinski, 1975; Kafi et al., 2002; Azadi, 2009). Rezaei
(2009) reported wide diversity among different accessions of Ira-nian barberries especially with respect to berry number in cluster,cluster number in 1-year-old shoot, anthocyanin level in fruit andfresh weight of fruit.
Common (European) barberry (B. vulgaris) has many culti-vars/varieties, one of which is a seedless type often called B. vulgarisvar. asperma and occasionally B. vulgaris ‘Asperma’ (Hatch, 2007;Azadi, 2009), B. vulgaris var. apyerna (Ahrendt, 1961) and B. orien-talis var. asperma (Sabeti, 1965; Browicz and Zielinski, 1975). Theorigin is unclear: Europe (Hatch, 2007) or Iran (Kafi et al., 2002).
The origins and relationship between seedless types haveremained unclear so far. Seedless barberry, whether Iranian orEuropean, has often been considered a variety and has been called“B. vulgaris var. asperma”, but some authors describe it as a cul-tivar under the name “B. vulgaris ‘Asperma”’ (Hatch, 2007; Azadi,2009). In addition, the name “B. vulgaris var. apyrena” is used forEuropean seedless type (Ahrendt, 1961) and Ghahreman (2001)believes that Iranian seedless cultivar is a member of B. khorasanica,which is considered a synonymous with B. vulgaris × B. integerrima(Azadi, 2009). Moreover, B. orientalis var. asperma is used (Sabeti,1965; Browicz and Zielinski, 1975). Despite all this, there are reli-able evidences indicating that Iranian seedless cultivar belongs toB. integerrima.
Heidary et al. (2009) studied genetic diversity and relationshipsamong Iranian barberries using AFLP markers. Cluster analysis byAFLP information placed Iranian seedless cultivar among ecotypesof B. integerrima. In addition, results of SSR and RAPD studiesfound Iranian seedless barberry to have a close relationship withB. integerrima (Rezaei et al., 2011; Sodagar et al., 2012). How-ever, none of these authors asserts that Iranian seedless barberryis a member of B. integerrima. There are also indirect evidences.Self-incompatibility is observed in both the seedless cultivar andwild B. integerrima, so that there were no seeds following self-pollination (Heidary, Unpublished; Ebadi et al., 2010), whereascommon barberry (B. vulgaris) can self-pollinate (Peterson, 2003)and may produce seeds. Common barberry is diploid (Minore andRudolf, 2008; Rounsaville and Ranney, 2010; Schlegel, 2010), whileIranian seedless cultivar and wild B. integerrima show tetraploidy(Sodagar et al., 2012; Heidary, Unpublished). Moreover, althoughKafi et al. (2002) stated that the lack of black stem rust infection inIranian seedless barberry grown in South Khorasan is due to the lackof warm and wet climate, this case may be another evidence statingthat Iranian seedless barberry is not a member of B. vulgaris that isthe most susceptible species (Peterson, 2003; Minore and Rudolf,2008; Berlin, 2012). Despite these evidences, no proper scientificname has been assigned until now. Accordingly, the name Berberisintegerrima ‘Bidaneh2’ is assigned for Iranian seedless barberry.
Nevertheless, there is another question to be answered care-fully: does the type of seedless barberry that is considered to have
originated in Europe (Hatch, 2007) have any relation with Iranianseedless barberry? As it is said that plants resulted from suck-ers of European seedless type produce fruits containing seed(s)
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Loudon, 1838; Richards, 1894; Darwin, 2010) and this case doesot hold true for Iranian seedless barberry, it could be suggestedhat they are different. It was claimed that seedlessness of Euro-ean seedless barberry is due to ontogenetic variation, because
t was reported to be evident only in old plants (Loudon, 1838;ichards, 1894). However, there is no scientific research study-
ng on the mechanism of seedlessness. Therefore, this hypothesishould be also of interest to researchers that European seedlessarberry may be a chimeric plant and developed from somaticutation(s). With respect to these uncertainties, any conclusion
annot be remarked. Clearly, more explicit and updated informa-ion is required.
. Origin and distribution
Berberis was probably originated before Palaeocene in Easternsia (Li et al., 2010). The genus has two centers of diversity, one Asia
or Eurasia) and another South America (Ahrendt, 1961; Landrum,999; Kim et al., 2004). Common barberry has Asian origin, most
ikely to be of Middle and Western Asiatic mountains (Kern, 1921;eterson, 2003). In some regions (e.g. United States), it is consid-red as an invasive and noxious weed (Minore and Rudolf, 2008).ntegrifolious barberry (B. integerrima syn. B. densiflora Boiss. &uhse; Zereshk-e Abi in Persian) is distributed over many parts of
ran (Parsa, 1986; Azadi, 2009). It is also found in Uzbekistan andyrgyzstan (Zaurov et al., 2013), Kazakhstan (Dzhangaliev et al.,003), Tajikistan (Davlatov and Baikova, 2011; Nowak and Nobis,013), Iraq, Turkey, Turkmenistan, Afghanistan, Pakistan, Kashmirnd Northwest of China (Parsa, 1986; Azadi, 2009). The backgroundf zereshk cultivation in Iran dates back to two century ago (Kafit al., 2002; Rezvani Moghaddam et al., 2013). Iran is the only coun-ry that produces seedless crop, commercially (Tehranifar, 2003;allahi et al., 2010). More than 95 percent of the crop is producedn South Khorasan province (Radmehr, 2010).
Birds (Herrera, 1982) and cattle (Kern, 1921) are distributive fac-ors for barberry seeds. It was noted that birds hasten germinationf the seeds when ingest and excrete fruits. Moreover, the lizardiolaemus bellii distributes Berberis empetrifolia (Celedon-Neghmeat al., 2008).
. Adaptability
In natural conditions, barberry seeds, after receiving coldequirements, begin to germinate in the spring. The germinations epigeal (Minore and Rudolf, 2008). Shaded place in the edge of
oodlands, alkaline and sandy-loam soils are the best conditionsor seed germination and survival of the seedling (Peterson, 2003).ommon barberry is a rhizomatous plant. The rhizomes, fromhich shoot arises, are produced continuously from the crown,
nd, thus, the parent bush increases its size. Root fragments arelso capable of reproduction (Peterson, 2003). In any kind of soil,arberries can be grown and developed (DeGraaf, 2002; Peterson,003; Arayne et al., 2007), and even Iranian seedless barberry canroduce an acceptable crop. This cultivar shows a good resistancegainst drought conditions. The quality of water and soil resourcesf many cultivating regions of Iran is poor; so that many of theands that are under cultivation of this crop are not suitable for
any other agricultural crops (Kafi et al., 2002; Zarkar, 2011). It is cold-hardy plant (Kafi et al., 2002) growing well in mountainousegions with cold winters. Summer heats in low-lying plains andot winds are limiting factors for the growth and crop production
Mahmoodi et al., 2009).
The bud break of Iranian seedless zereshk occurs at late March15–18 ◦C (Kafi et al., 2002)]. About 97.5 degree days are requiredor flowering (Fallahi et al., 2010), which is received after about
nd Products 50 (2013) 276– 287
30–40 days. Thereby the plant flowers in the temperature rangeof 19–23 ◦C (Kafi et al., 2002). Depending on genotypes and envi-ronmental conditions, flowering of barberries occurs at early May[Iranian seedless barberry (Fallahi et al., 2010)], May to June [B.vulgaris (Viertel, 1970; Peterson, 2003)] or April to June [B. vul-garis (DeGraaf, 2002; Minore and Rudolf, 2008)] taking about 20days in Iranian seedless barberry (Kafi et al., 2002). Hermaphroditeflowers of barberry are borne on racemes located on shoots pro-duced in the preceding year (Ebadi et al., 2010). Cold injuryoccurs rarely in the blooms (Kafi et al., 2002). Pollens are stickyand produced in small amounts (Cadic, 1992). The nectar at thebase of each petal attracts insects (i.e. bees, wasps, ants, filesand beetles) that are the most common pollinators for barberryflowers (Peterson, 2003). Although Cadic (1992) suggested that“Berberis is also self-fertile and mainly autogamous”, some typesshow self-sterility and cross-pollinating (Anderson et al., 2001;Peterson, 2003; Heidary, Unpublished). Seismonasty of stamens(Cadic, 1992), movement of the insects among flowers and touch-ing filaments make pollens to dehisce on the insect’s body. Thus,the insect facilitates pollination by touching receptive stigmas. InIranian seedless barberry, small berries can be seen at mid to lateMay [in common barberry at July (DeGraaf, 2002)]. They beginto turn in color at mid July (Fallahi et al., 2010) or mid to lateAugust (Kafi et al., 2002). Until early August (Fallahi et al., 2010)or early September (Kafi et al., 2002), the color turns from greento purple or red. Thermal requirement of Iranian seedless bar-berry is about 1530 degree days from flowering stage to ripeningand harvesting fruits (Fallahi et al., 2010). Fruits may be damagedby early autumn chilling (Mahmoodi et al., 2009). Vegetative andgenerative periods take about 220–235 days and subsequently dor-mancy is induced with drop of temperature to 7–11 ◦C (Kafi et al.,2002).
Common barberry is adapted to cross-pollination but it canalso self-pollinate (Peterson, 2003). However, Iranian seedless bar-berry does not produce seed by self-pollination mainly because ofgametophytic self-incompatibility, which is also evident in wildB. integerrima. In addition, incomplete ovules and unfused polarnuclei (lack of endosperm) are also observed in the seedless cul-tivar; therefore, by cross-pollination, only 20–30% of the fruitsdevelop seed(s), whereas wild B. integerrima develop seed(s) inabout 90% of the fruits (Ebadi et al., 2010; Heidary, Unpublished).Rezaei et al. (2011) stated that Iranian seedless barberry couldbe developed through spontaneous mutation(s) [but not to resultself-incompatibility system, perhaps to cause incomplete ovulesand/or disturbance in forming endosperm]. However, incompleteovules phenomenon is also observed in B. crataegina (Ebadi et al.,2010), and so this may also be incorrect. Ebadi et al. (2010)reported that fruit set in the seedless cultivar is due to stimu-lative parthenocarpy. However, Heidary (Unpublished) observedthat fruit set was about 33% and 40% in covered emasculated andcovered intact flowers, respectively. Nonetheless, results of Ebadiet al. (2010) are questionable, since pollination of emasculatedflowers with self pollens resulted in a very lower fruit set (27%),compared to that of covered intact flowers (72%). Is it really pos-sible for male parts of flowers and/or petals to have produced achemical that stimulated fruit set? Based on these findings, anyconclusion could not be remarked firmly, but vegetative partheno-carpy may be suggested as the primary reason for fruit set inIranian seedless barberry, though a better fruit set may followpollination.
5. Propagation
Although harvested ripe fruits may be sown immediately(DeGraaf, 2002), because of a resting period, the seeds should
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e extracted and allowed to dry and then placed into moistands with cold temperatures for about 15–90 days, depending onenotype and climatic conditions (DeGraaf, 2002; Piotto and Di Noi,003; Peterson, 2003; Rezaei and Balandary, 2013). One reasonor the superiority of extracted seeds may be the fruit infesta-ion of molds resulting in loss of seeds in it (Minore and Rudolf,008). It is reported that GA3 had significant positive effect on B.
ntegerrima seed germination, but it was not effective as much asold-stratification (Rezaei and Balandary, 2013). Norozi et al. (2011)ound that fresh seeds of B. integerrima had better germination com-ared to 1-year-old those. Longevity of common barberry seeds iseported to be up to 11 years (Peterson, 2003). They can be keptn sealed containers (DeGraaf, 2002) with a temperature range of–3 ◦C at least for 4 years. Thus, they are orthodox in keeping con-ition (Minore and Rudolf, 2008).
In Iran, all orchards of Iranian seedless zereshk are establishedrom sucker propagation (Kafi et al., 2002; Tehranifar, 2003; Rezaeit al., 2011). Two- to three-year-old suckers are divided fromother plants at mid to late November. They should have 60–70 cm
ength and adequate roots (Kafi et al., 2002). However, it is veryime consuming and expensive, and the number of suitable suck-rs is limited. In addition, it may cause some damages to motherlants that are producing crop.
Common barberry can be propagated by cutting, layering,rafting and sucker (DeGraaf, 2002; Minore and Rudolf, 2008).n addition, European seedless barberry can be propagated byutting and sucker; however, some authors claimed that plantsesulted from suckers would produce seeded fruits (Loudon, 1838;ichards, 1894; Darwin, 2010). Nevertheless, Iranian seedless bar-erry is a difficult-to-root cultivar and the studies on rooting of
ts cuttings have not been enough successful yet. Softwood, hard-ood and semi-hardwood cuttings treated with IBA, NAA and
heir mixture, Agrobacterium rhizogenes suspension, etc. have notooted (Tahanian and Razavi, 2000; Kafi et al., 2002; Azizi et al.,007).
Attempts to propagate Iranian seedless barberry through micro-ropagation and tissue culture methods have not also been muchuccessful yet. Use of A. rhizogenes on rooting of micro-cuttings inS medium did not have any promising result (Azizi et al., 2007).
here is only one successful report (Mohammadi et al., 2011). Theest callusing was observed with leaf sections (1–1.5 cm2) culturedt May and June. MS medium with 8 g L−1 agar improved callusormation compared to other evaluated media. The callus forma-ion significantly increased by treating 10 mg L−1 of 2,4-D, NAA andspecially Picloram.
There is no scientific report about grafting Iranian seedless bar-erry cultivar and it is also not common among traditional growers.owever, some grafted plants were observed in Khong village (Bir-
and). The grafting type was recognized to be saw-kerf (notch) orark grafting (Kafi et al., 2002). Nevertheless, grafting and buddingethods seem to provide solutions for propagating Iranian seedless
arberry but require experiments.
. Planting
Before planting, the land is plowed deep. Then it undergoesisking and after that the holes (50 cm × 50 cm × 50 cm) are dugTehranifar, 2003). Planting suckers at mid autumn is more suit-ble than in the spring or at late winter (Kafi et al., 2002;ehranifar, 2003). In South Khorasan, shrubs are mainly plantedith 4 m × 4 m, 4 m × 5 m and 5 m × 5 m distances (Kafi et al., 2002).
ence, there are about 400–625 plants per hectare. It is reported
hat 1666 shrubs per hectare (with 2 m × 3 m spacing) produced theighest crop yield in Iranian seedless barberry (Mokhtarian et al.,011, 2012).
nd Products 50 (2013) 276– 287 279
7. Training and pruning
Many traditional growers do not follow a regular training sys-tem on shrubs whereby the shrubs become crowed, gradually. Theresult would be a decrease in yield and quality of the crop as well assome troubles in horticultural operations (Kafi et al., 2002). Pruningis only limited to remove very old and/or diseased branches (Kafiet al., 2002; Tehranifar, 2003).
Kafi et al. (2002) described the trial conducted by Balandary(2000). He compared the single- (tree like) and multiple- (shrublike) trunk training systems with the traditional training method.Single-trunk method resulted in easier managmential operationsand harvest. It also reduced ruination of the crop in comparison tothe traditional method. Furthermore, this method is more adaptedto mechanical harvesting by shaker and decreased the zereshk twigborer population due to the limitation of suitable sites for the layingeggs (Balandary, 2000; Mokhtarian et al., 2011, 2012). However, itis costly and time consuming. Multiple-trunk training method ismore adapted to the behavior of the shrub. It increases the photo-synthetic efficiency and so makes berries larger. This method is alsoresulted in an easier harvest and lower crop losses in comparisonto the traditional method (Balandary, 2000).
8. Irrigation
Generally, barberry is a resistant/tolerant plant to drought con-ditions (Kafi et al., 2002). However, water deficit in soil can causea sharp reduction in yield. For obtaining an acceptable yield,irrigation is important during petal fall until one week before har-vest (Tehranifar, 2003). Traditional growers believe that irrigationshould not be excessive in flowering period, as may result in flowerdropping, thus reducing yield of the final crop (Kafi et al., 2002).
For the establishment of shrubs, growers irrigate plants every 7or 8 days during the first few years. After the establishment of plantsand the beginning of fruiting, the shrubs are usually irrigated with12–15 days intervals, depending on climatic and soil conditions.For example, in some mountainous regions, the orchards are notirrigated more than 3–4 times during growing season (Kafi et al.,2002). In an irrigation trial under a clay soil, yield was not signifi-cantly reduced when irrigation intervals stretched out from 8 to 12days. In addition, 16 days intervals reduced the yield only by 6%;therefore, it was the best treatment for watering respecting watershortage of the region (Kafi et al., 2002). Iranian seedless zereshk issomewhat tolerant to saline water (Tehranifar, 2003).
9. Fertilization and manuring
Iranian seedless barberry is a low nutrient demanding plant;however, it requires nutrition for a better crop yield (Kafi et al.,2002). It is recommended to incorporate about 35–70 tonnesof barnyard manure, and 100, 100 and 50 kg/ha of N, P2O5 andK2O (respectively) before planting (Tehranifar, 2003). Althoughthere has been no investigation about requirement of the threemain nutrients (i.e. nitrogen, phosphorous and potassium), nativegrowers apply about 100 kg/ha of urea fertilizer in early spring and150 kg/ha of ammonium phosphate in the autumn or late winter(Kafi et al., 2002). In an experiment, Khayyat et al. (2008) studiedthe effect of foliar application of manganese, boron, potassium, cal-cium and zinc. Vitamin C and soluble solids content were increasedby spraying calcium 3% and potassium 2%, respectively; however,the highest yield was obtained by spraying water (referred to
as control). They interpreted that the increase of yield resultedfrom spraying water is because of its positive effect on effectivepollination period by increasing the humidity of the stigmas.However, it seems that it is an incorrect interpretation, because
280 A. Alemardan et al. / Industrial Crops and Products 50 (2013) 276– 287
Table 1Pests that attack Iranian seedless barberry.
Pest Host Control Natural enemy Reference
Barberry twig borerSyrista parreyssi (Spin.)
Iranian seedlessbarberry
Pruning shoots and suckersinfected by the eggs
– Anbarani (1991) and Kafi et al. (2002)
EarwigForficula tomis (Kolenati)
Iranian seedlessbarberry, apple,and cucurbits
Carbaryl around crown,removing stubbles andundesirable stems and suckers
Calathus sp. Kafi et al. (2002) and Rahimi et al.(2011)
Gypsy MothLymantria dispar (L.)
Wide Host range Tying lacy fabrics aroundshrubs, insecticides
Large number Anbarani (1991) and Hoover (2001)
Lackey MothMalacosoma neustria (L.)
Wide Host range Pruning shoots infected by theeggs, organophosphoruspesticides in the larval stage
Kalushkov (1998), Kafi et al. (2002) andWojciechowicz-Zytko and Jankowska(2011)
Fruit FlyRhagoletis berberidis, R.meigenii
Berberis spp. Autumnal plowing, Noeconomic damage on Iranianseedless barberry
Habrocytus sp. Anbarani (1991) and Stibick (2004)
Olive ScaleParlatoria oleae (Colv.)
Wide Host range No economic damage onIranian seedless barberry
Aphytis maculicornis Rosen (1977) and Kafi et al. (2002)
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Barred Fruit-tree TortrixPandemis cerasana(Hubner) syn. P. ribeana
Wide Host range No economic damageIranian seedless barb
he treatments were applied 15 days after fruit set. It could beuggested that precise researches be carried out to clear barberryertilizer requirement.
0. Biennial bearing
Although it is generally said that barberries produce good croplmost annually (Minore and Rudolf, 2008), biennial bearing is aritical issue in the production of Iranian seedless zereshk. In firstears of the orchard establishment, it is insignificant but increasesith the age and becomes evident 20 years afterwards (Kafi et al.,
002). In a 5-year-long study on a commercial orchard, fruitingate fluctuations were determined to be even more than 40%. Its accordingly the reason why some growers tend to cancel fruitarvesting in the off year (Rezaei and Balandary, 2011).
There is no report about the exact mechanism of biennial bear-ng. However, because of lacking seed in fruits, it seems that it islmost associated with carbohydrate depletion. Crop harvestingethods (see Section 13.2) have great influences on the biennial
earing. Harvesting by beating shoots can aggravate this issue dueo breaking young twigs, which are places for flowering of the nextear. Additionally, cutting fruiting shoots removes much of thetored carbohydrates. Stored carbohydrates are also affected by theanagmential procedures such as training, pruning and nutrition.ibberellic acid is reported to quench biennial bearing (Balandary,995).
1. Gibberellic acid application
Spraying 200 ppm gibberellic acid (GA3) at full bloom and again5 and 30 days later improved fruit set and fruit weight in Berberissiatica (Minore and Rudolf, 2008). Balandary (1995) also studiedhe effect of spraying gibberellic acid (25, 50, 100 and 200 ppm)
t full flowering and after petal falling in Iranian seedless zereshk.he highest berry weight was achieved by spraying 200 ppm at fullowering stage but the leaves and young shoots became abnormal.herefore, 100 ppm is reported to be the best concentration. Inter-stingly, gibberellic acid also caused a higher fruit set in the nextear (off year) and, thus, partly balanced biennial bearing.
Agathis montana Kafi et al. (2002) and Guclu and Ozbek(2007)
12. Pests and diseases
Little attention has been paid on the pests and disease of Ira-nian seedless barberry. Kafi et al. (2002) studied most of the pests(Table 1) and diseases (Table 2) and most of the information comesfrom their experiments.
13. Yield and harvesting
Climatic conditions, managing operations, date and method ofharvest, and size and age of the shrub could be effective on berryyield per shrub (Fallahi et al., 2010; Rezvani Moghaddam et al.,2013). Moreover, fruiting of Iranian seedless barberry is biennial(see Section 10). Generally, the cultivar begins to fruit 3 or 4 yearsafter planting suckers, and a 7-year-old orchard should produceabout 2 tonnes of dried crop per hectare in suitable conditions andin on year (Kafi et al., 2002; Tehranifar, 2003).
Harvesting is one of the most difficult steps in the productionof barberry crop; because shrubs have many spines in their denseshoots (Fig. 1) and the fruit peel is thin (Balandary, 1995; Kafi et al.,2002).
13.1. Date and time of harvesting
Predicting the desired harvest date is important in yield andquality determination of the crop. For this, native growers use somesensory properties such as changing fruit color from bright to darkred, softening the tissue, concentrating the contents (more pasti-ness sense when the fruits are squeezed between the fingers) anddecreasing fruit sourness (Kafi et al., 2002).
The best harvest time for barberry is a time when the berrieshave ripened by autumnal cold. On the effect of ripening, thefruit becomes dark red (higher anthocyanin) and the sournessand berberine content reduce, while sweetness increases (Chandraand Todaria, 1983; Minore and Rudolf, 2008; Arena and Curvetto,2008; Mahmoodi et al., 2009; Rezvani Moghaddam et al., 2013).For instance, anthocyanin content increased about 2.5 times by
delaying the harvest from 10 September to 13 November (RezvaniMoghaddam et al., 2013). Although quality and yield of the cropwill increase by delaying harvest, if it is delayed too long, the cropmay be injured by early autumn chilling (Mahmoodi et al., 2009)
A. Alemardan et al. / Industrial Crops and Products 50 (2013) 276– 287 281
Table 2Diseases that attack Iranian seedless barberry.
Disease/disorder Causing factor Host Control Symptom/Sign Reference
Partial change in fruit color Unknown Iranian seedlessbarberry
– Hollowing of the palefruits
Kafi et al. (2002)
Flattened stems Unknown; Probably avirus
Iranian seedlessbarberry
Pruning with sterilizedsecateurs
Flatting of strongstems, abnormalfoliage
Kafi et al. (2002)
Mottled leaves lower Unknown; Probably abacterium
Iranian seedlessbarberry
– Roundish brown stains,early drying of fruits
Kafi et al. (2002)
Wrinkled and dried fruits Unknown; Probably abacterium
Iranian seedlessbarberry
– Dark stains on leavesoften before fruitripening
Kafi et al. (2002)
Powdery mildew Microsphaera berberidis(DC. Ex Merat)
Different members ofBerberidaceae
Pruning infectedbranches, fungicides
White colored myceliaon leaves
Kafi et al. (2002) andGlawe (2003a,b)
Cereals black stem rust Puccinia graminis(Pers.)
365 species of cerealsand grasses, and manyBerberis species(Iranian seedlessbarberry not reportedyet)
Pruning infectedbranches, fungicides
Protuberant roundstains on (pycniaclusters) and under(aecia clusters) leaves
Leonard and Szabo(2005) and Berlin(2012)
Witches’ broom forming rust Puccinia arrhenatheri Arrhenatherum spp., Pruning infected Many small branches Naef et al. (2002) and
ac
TcbHswis4ihMr
mimmrm
(Kleb.) Erikss Berberis spp.
nd drying operations may not properly be done if autumnal pre-ipitation begins (Kafi et al., 2002; Fallahi et al., 2010).
Fruit development and maturation varies with different regions.herefore, the suitable harvest date should be experimented in theertain region. In mountainous regions with colder climates, bar-erry fruits become red sooner than those in warmer climates do.owever, respecting the yield, Mahmoodi et al. (2009) found that
uitable harvest time is later in the colder region than that in thearmer one. In South Khorasan, about 170 days after full flower-
ng may be a suitable criterion for harvesting the crop of Iranianeedless zereshk. It is also reported that maturity index values of.5–5 are good measures for determining suitable date for harvest-
ng crop of Iranian seedless zereshk (Kafi et al., 2002). In addition,arvest time in the day influences barberry fruits quality. Rezvanioghaddam et al. (2013) reported that fruits harvested before sun-
ise had higher quality compared to those harvested at noon.However, due to the lack of special stores and modern drying
achines, to prevent losing the crop caused by autumnal precip-tations and damages by birds, growers in Ghaen harvest crop at
id October, while Fallahi et al. (2010) reported that physiologicalaturity were continuing at least until mid November in the same
egion. Furthermore, because of labor issues, harvesting at earlyorning cannot be currently feasible in large-scale cultivations.
Fig. 1. Spiny habit of the barberry shrub.
branches, fungicides on the main stems,yellowness of theleaves
Kafi et al. (2002)
13.2. Methods of harvesting
Three methods are used for harvesting Iranian seedless bar-berry berries (Kafi et al., 2002; Tehranifar, 2003; Alavi andMazloumzadeh, 2012). Cutting fruiting shoots: fruiting shoots arecut from the junction of the main stem by secateurs. About 13–17 kgof fresh fruits are taken from 15 to 20 kg of harvested fresh shoots(Fallahi et al., 2010). Picking fruit clusters: fruit clusters are hand-harvested one by one. Beating shoots: a thick fabric is put underthe shrub, and the shoots are beaten by long sticks.
Harvest method can have significant influence on crop qualityand biennial bearing (see Section 10). Crop quality is determinedby various criteria (e.g. color, density, foreign material level, moldcontamination status, etc.). They are affected by harvest methods.Harvesting fruit bearing shoots causes a crop with lower density(more puffy berries) and, thus, enhances crop quality (Kafi et al.,2002; Alavi and Mazloumzadeh, 2012). In the basis of crop qualityindices (e.g. soluble solids, total titratable acidity, maturity indexand anthocyanin content of fruit), Rezvani Moghaddam et al.(2013) reported that berry picking method is better than cuttingfruiting shoots. However, in current condition, because of spines,this method is time consuming and needs skilled laborer (Kafiet al., 2002). In addition, beating shoots method damages youngshoots and results in berries with lower quality (fruits collidewith spins). Therefore, it is the worst harvest method (Balandary,1995; Kafi et al., 2002; Tehranifar, 2003). Unfortunately, thedominant harvest method in Iran is still beating shoots (Alavi andMazloumzadeh, 2012).
14. Crop quality
Water activities, microbial load and growth of microorgan-isms, enzymatic activities and changing pigments caused byoxidation are the most important factors influencing negativelybarberry crop quality (Valipoor Motlagh et al., 2009; Moradi andMohamadi-Sani, 2011). Enzymes in the barberry fruits (pheno-lases and polyphenolases) are released after fruit is harvested.They make browning of the crop, thus reducing apparent as well
as dietary quality through attacking the anthocyanin pigments(Kafi et al., 2002). Poor appearance and high microbial load havebeen crashing global markets for Iranian seedless zereshk berries(Moradi and Mohamadi-Sani, 2011).
2 rops and Products 50 (2013) 276– 287
ivhRiha(2cM
siai
aiomfe2
rbupb
maisM
1
pmiiwR
sADd(i2
Asdftamwa
They are rich in vitamin C almost matching citrus fruits in thisrespect (Table 3). In Iran, dried berries are used as food additives inmany dishes (e.g. a popular meal called “Zereshk-Polow Ba Morgh-
82 A. Alemardan et al. / Industrial C
Anthocyanin content is also considered as a qualitative index. Its affected by climate, harvest date and time in the day. Late har-esting and harvesting at morning make anthocyanin level to beigher in comparison to early harvesting and harvesting at noon [i.e.ezvani Moghaddam et al. (2013) reported 34% increase by delay-
ng harvest from 23 October to 13 November, and 50% decrease witharvesting at noon in comparison to at early morning]. Moreover,nthocyanin accumulation is higher and begins earlier in elevatedcolder) regions compared to in warmer regions (Mahmoodi et al.,009). It is reported that reduced anthocyanin content in warmerlimates is due to its instability in higher temperatures (Rezvanioghaddam et al., 2013).Soluble solids content (SSC, determining sweetness) is also con-
idered a qualitative index. In colder regions, it is higher than thatn warmer regions. Mahmoodi et al. (2009) reported that SSC wasbout 21–26.5% in the colder region, while it was about 17–22.1%n the warmer region.
Mechanical damages occurring during harvesting, transportingnd storing operations seriously reduce barberry crop quality. Beat-ng shoots harvest method has an important role in the occurrencef such a low quality (Kafi et al., 2002). Blanching is a suitable treat-ent for reducing damages caused by enzymatic activities in the
ruits. Treating berries with hot water of 80 ◦C for 1 min inactivatesnzymes, thus inhibiting the deterioration of quality (Kafi et al.,002).
Rajaei and Noorbakhsh (2008), to monitor crop quality inespect to foreign material amounts, studied the correlationetween results of image processing technique and sensory eval-ations made by experienced persons. They reported that imagerocessing technique could be a useful method for evaluation ofarberry crop quality.
Level of puffy fruits is another qualitative index, so that theore puffy the fruits, the higher quality (Kafi et al., 2002; Alavi
nd Mazloumzadeh, 2012). Dourandish et al. (2011) found that thisndex is the most important quality index in Birjand. Fruit den-ity is a useful criterion for puffy fruits level evaluation (Alavi andazloumzadeh, 2012).
5. Drying
The most important purpose of drying barberry berries is torevent them from rotting during storage period. However, it alsoakes an easier and more efficient packaging and transporting. It
s said that drying should be continued until the moisture of fruitss reduced to about 20% (Kafi et al., 2002). About 1 kg of dried fruit
ould be obtained from each 3 kg of fresh fruits (Fallahi et al., 2010;ezvani Moghaddam et al., 2013).
Three methods are used for drying barberry berries: sun drying,hade drying and drying using cabinet dryers (Fallahi et al., 2010;lavi and Mazloumzadeh, 2012; Rezvani Moghaddam et al., 2013).rying process takes about 10–15 days under sunlight and 14–25ays under the shade of the autumn (Kafi et al., 2002). Industrialcabinet) dryers have recently been developed to shorten the dry-ng period and to enhance crop quality (Alavi and Mazloumzadeh,012).
Native growers often dry fruits under sunlight (Tehranifar, 2003;lavi and Mazloumzadeh, 2012). Alavi and Mazloumzadeh (2012)tudied the effects of these three methods (industrial drying wasone in a laminated cabinet with a temperature range of 55–60 ◦Cor 20 min) on crop quality. Evaluation of colorimetric parame-ers showed that industrially and sun dried berries had the lowest
nd the highest redness, respectively. Berries dried with industrialethod had higher brightness. The lowest and the highest densityere observed in sun and industrially dried berries, respectively. In
ddition, rapid drying made by industrial method wrinkled berries.
Fig. 2. Barberry berry is often sold in bulk.
However, according to panelists (evaluating tissues, color, smell,taste and general appearance), shade dried berries were the best.Rezvani Moghaddam et al. (2013) reported that sun drying is a sat-isfactory system. Interestingly, anthocyanin level in sun dried fruitswas two times higher than that measured in shade dried fruits (72compared to 35 mg/100 g dry berries, respectively).
16. Packaging
In general, the package, whatever it might be, should maintainredness of barberry fruits, be transparent for ensuring customerthat the crop has a high quality, keep moisture content at thestandard level, be cheap and prevent penetration and growth ofmicroorganisms (Kafi et al., 2002). Unfortunately, modern tech-nologies are not currently used in Iran for packaging zereshkberries. This may be one of the reasons for the poor global mar-ket. In Iran, there is very little packaged barberry berries and mostof the crop is sold in bulk (Fig. 2).
Valipoor Motlagh et al. (2009) reported that packages contain-ing silver nanoparticles are suitable for packaging zereshk berries.They observed that zereshk fruits in packages containing 1% and2% concentrations of silver nanoparticles showed lower microbialgrowth compared to those stored in polyethylene packages andpackages with lower concentration (200 ppm) of silver nanoparti-cles. Furthermore, berries in those packages were also redder andbrighter.
17. Benefits
Every part of the barberry plants is used in some way (food,medicinal and industrial). In addition, some species (e.g. commonbarberry and Japanese barberry) are suitable shrubs for ornamen-tal purposes (DeGraaf, 2002). Shining red berries of the commonbarberry persist over winter and make a beautiful view.
17.1. Food uses
The fruits are consumed raw or cooked (Arayne et al., 2007).
e Za’farani3”). In addition, they are sometimes used for producing
3 Barberry Pilaf with Saffron Chicken.
A. Alemardan et al. / Industrial Crops and Products 50 (2013) 276– 287 283
Table 3Nutritionally comparison of Iranian seedless barberry with some other fruits.
Crop Anthocyanin (mg/100 g) Vitamin C (mg/100 g) Reference
Iranian seedless barberry 19–153 26–76 Rezaei (2009), Fallahi et al. (2010) and Rezvani Moghaddamet al. (2013)
Citrus – 31–77 Ortiz (2002)
fb
1
tnpwtEt(ii(bA
fiHpi(t(flwe
TD
Pomegranates 3–140 –
Blueberries 61–320 –
ood products, e.g. sauces, jellies, candies, concentrates, juices, car-onated beverages, jams, marmalades, etc.
7.2. Medicinal uses and effects
The use of barberry in folk medicine as a natural remedy for thereatment of a variety of diseases dates back to over two millen-ia ago. Ancient Egyptians used it with fennel seeds to preventlagues (Arayne et al., 2007). Medicinal properties of barberryere described in Babylonia about 650 BCE. By the seventh cen-
ury CE, the berries were a common therapeutic in the Middleast (Peterson, 2003). In traditional medicine, this plant was usedo cure such diseases as infectious fevers, typhus and diarrheaEbrahimi-Mamaghani et al., 2009). In vitro and in vivo studiesndicate pharmacological activities including antimicrobial, antiox-dant, anti-diabetic, hepatoprotective, and antihypertensive effectsTable 4). Medicinal uses and activities of Berberis vulgaris anderberine, its major active component, have been reviewed byrayne et al. (2007).
Alimirzaee et al. (2009) in studies of Staphylococcus aureusound that B. integerrima fruit extract enhanced antibacterial activ-ty of ampicillin with 1-methyl malate as the active component.adaruga et al. (2010) studied antioxidant activities of differentarts of B. vulgaris. Leaves and fruits had the best antioxidant activ-
ties, which were close to the antioxidant activities of quercetin1.5 mM) and vitamin C (1 mM). Higher antioxidant activities ofhe leaves and fruits are probably due to the phenolic compoundsanthocyanins) and ascorbic acid, which have high contents in the
ruits (Table 3). However, cannabisin G and (±)-lyoniresinol iso-ated from root bark of B. vulgaris have shown antioxidant activities
ith IC50 values of 2.7 and 1.5 �g mL−1, respectively (Tomosakat al., 2008).
able 4ifferent pharmaceutical effects of Berberis vulgaris and B. integerrima.
Effect Reference for fruit
Anticancer Motalleb et al. (2008)
Anticholinergic Shamsa et al. (1999) and KhosrokhavAnticoagulant –
Anti-colitis Minaiyan et al. (2011)
Anticonvulsant –
Antihistaminic Shamsa et al. (1999) and KhosrokhavAntihypertensive Fatehi et al. (2005) and Fatehi-HassaAnti-inflammatory Kiasalari et al. (2011)
Antimicrobial Alimirzaee et al. (2009)Anti-nociceptive, sedative Fatehi et al. (2005)
Antioxidant Motalleb et al. (2005) and Hadaruga
Anti-urolithiasis –
Decreasing morphine dependence andreinforcement
Nassiri-Asl et al. (2007) and Hashem
Hepatoprotective Jamshidzadeh and Niknahad (2006) a(2008)
Hypoglycemic, anti-diabetic Mirbadalzade and Shirdel (2011) and
Neuroprotective Fatehi et al. (2005)
Reducing LDL and total cholesterol Farhadi et al. (2008), Ebrahimi-MamMirbadalzade and Shirdel (2011) and
Hernandez et al. (1999), Kulkarni and Aradhya (2005),Alighourchi et al. (2008) and Sepulveda et al. (2010)Vollmannova et al. (2009)
Fatehi et al. (2005) reported that the administration of B. vulgarisfruit extract reduced mean arterial blood pressure and heart ratein rats, thus validating the use of barberry fruit as an antiarrhyth-mic agent in traditional Iranian medicine. The extract enhancedmagnitude of the outward potassium current in cells present in thebrain slices of parabrachial nucleus and cerebellum. Fatehi et al.(2005) report that the sedative effects (known in traditional Ira-nian medicine) and neuroprotective effects of barberry may be dueto this mechanism.
A number of studies report anti-diabetic activities of barberryfruit and other organs. Meliani et al. (2011) reported anti-diabeticactivities of aqueous extract of the root bark and saponins extractedfrom the root bark. They suggested that anti-diabetic activity ofthe root bark may be due to saponins. However, berberine, whichoccurs mainly in the root and stem barks, is well documented forits anti-diabetic effect (Yin et al., 2012 and references therein).Shidfar et al. (2012) reported significant decrease in serum triglyc-eride, total cholesterol, LDL-c, apolipoprotein B, glucose, insulin,and insulin resistance and significant increase in total antioxidantcapacity in response to the administration of B. vulgaris fruit extract.They interpreted the anti-diabetic effect to be mainly due to berber-ine. However, ripe barberry fruit has a very lower content of thisalkaloid compared to the root and stem barks. Therefore, there maybe (an)other mechanism(s) for anti-diabetic activities of barberryfruits. In addition, some studies report that the fruit (Jamshidzadehand Niknahad, 2006; Motalleb et al., 2008) and root (Fallah-Huseiniet al., 2010; Taheri et al., 2012) protect liver against chemical dam-ages.
17.3. Active components
Among active components of barberry, the alkaloid berberine(Fig. 3) occurring in bark of root, stem and unripe fruit is considered
Reference for plant
–ar et al. (2010) –
Hosseinzadeh and Razieh (2011)–Hosseinzadeh et al. (2012)
ar et al. (2010) –nabad et al. (2005) Azmat et al. (2009)
Mohebali et al. (2011)Meshkibaf et al. (2010)Mohebali et al. (2011)
et al. (2010) Tomosaka et al. (2008), Hadaruga et al. (2010)and Pogacnik and Ulrih (2011)Bashir et al. (2010)
zaei et al. (2012) –
nd Motalleb et al. Fallah-Huseini et al. (2010) and Taheri et al.(2012)
Shidfar et al. (2012) Meliani et al. (2011) and Ahangarpour et al.(2012)–
aghani et al. (2009), Shidfar et al. (2012)
Meliani et al. (2011)
284 A. Alemardan et al. / Industrial Crops a
O
O
ON+
t2HgedboAiCtaa
(ftmle(2rmeiae
1
iItf1ecFr2ew2
1
g
O
Fig. 3. Chemical structure of berberine.
he most important active constituent of this plant (Arayne et al.,007). Berberine, a yellow colored bitter substance (Panda, 2005;anson, 2003; Arayne et al., 2007), belongs to a large and diverseroup of alkaloids called benzylisoquinolines (Kutchan, 1995; Zulakt al., 2006; Klein and Roos, 2009). The yellow color of the plant isue to this alkaloid (Panda, 2005). The highest concentration oferberine was found in bark (∼6%) and root (3.8%); and the lowestccurrence was found in leaves and fruits (Hadaruga et al., 2010).rayne et al. (2007) report the highest level in root bark. Berberine
s found not only in Berberis species, but also in Argemone mexicana,optis chinensis, Coptis japonica, Coptis teeta, Coscinium fensetra-um, Hydrastis canadensis, Mahonia aquifolium, Thalictrum minus,nd Toddalia aculeata (Zulak et al., 2006; Barceloux, 2008; Kleinnd Roos, 2009).
Pharmaceutical effects of berberine have been widely reportedSiow et al., 2011; Yin et al., 2012). Berberine is well documentedor its effects in treating diabetes (Yin et al., 2012 and referencesherein). It displays antimicrobial activity, for example against
ulti-drug resistant Escherichia coli (Bandyopadhyay et al., 2013),ipid-lowering effects (Hu et al., 2012), anti-cancer activity in sev-ral kind of cancer including esophageal (Iizuka et al., 2000), lungPeng et al., 2006), breast (Kim et al., 2010), bladder (Yan et al.,011), and prostate (Wang et al., 2012), and also protects againstadiation-induced lung injury (Liu et al., 2008). Berberine may beore effective than doxorubicine in treating breast cancer (Kim
t al., 2010). Moreover, berberine has been reported to be a promis-ng agent for the treatment of Alzheimer’s disease (Asai et al., 2007)nd active against human immunodeficiency virus [HIV (Bodiwalat al., 2011)].
7.4. Other uses
Barberry is also used for dyeing wool, silk and cotton, whichs helpful for sustainability of the environment (Kafi et al., 2002;mani et al., 2011). In addition, in vitro and in vivo studies showedhat extract of the plant could be a biologically controlling agentor fire blight caused by Erwinia amylovora (Mosch and Klingauf,989; Mosch et al., 1990; Psallidas and Tsiantos, 2000) and the barkxtract has significant negative effect on Botrytis cinerea, whichauses great economic losses of crops every year (Parvu et al., 2010).urthermore, powdered dried roots and dried fruits of barberryepresented beneficial effects in poultry production (Rajaian et al.,003; Kermanshahi and Riasi, 2006). Moreover, berberine may beffective in controlling brown rot caused by Monilinia fructicola,hich causes considerable yield reduction of peaches (Hou et al.,
010).
8. Conclusion
Iranian seedless barberry (B. integerrima ‘Bidaneh’) is propa-ated only from sucker. This method has disadvantages and cutting
nd Products 50 (2013) 276– 287
propagation may also not have good results. Therefore, it is stronglysuggested that trials be carried out on budding and grafting. Nutri-tion requirement is not investigated. Regarding sustainability of theenvironment, it is important to study about nutrition requirementand it will accordingly be possible to reduce environmental pollu-tion using appropriate amount of fertilizers. Biennial bearing is agreat issue in the production of Iranian seedless barberry crop, butthere has been no special study about the mechanism and findingsolutions. The plant is very spiny which is a problem. Therefore,efforts should be made to develop new genotypes having no orat least lesser spines. Barberries are valuable multipurpose plants.Despite the many benefits, there is a critical problem. Many speciesof Berberis play as alternate hosts for the rust fungi (Puccinia spp.)and they can thus indirectly cause great damages to cereals. There-fore, barberry plants must be avoided in cereal producing areas.
Acknowledgment
We would like to sincerely thank Professor Jules Janick for hisinvaluable guidance in writing and revising the present article.
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