Review Abiotic stresses, constraints and improvement ... · molecular breeding (MB) approaches...

Review

Abiotic stresses, constraints and improvement strategies in chickpeaU D A Y C . J H A

1, S U S H I L K . C H A T U R V E D I1, A B H I S H E K B O H R A

1, P A R T H A S . B A S U1, M U H A M M A D S . K H A N

2

and D E B M A L Y A B A R H3,4

1Indian Institute of Pulses Research (IIPR), Kanpur, 208024, Uttar Pradesh India; 2Centre for Agricultural Biochemistry andBiotechnology, University of Agriculture, Faisalabad, Pakistan; 3Centre for Genomics and Applied Gene Technology, Institute ofIntegrative Omics and Applied Biotechnology (IIOAB), Nonakuri, Purba Medinipur, West Bengal 721172, India; 4Correspondingauthor, E-mail: [email protected]

With 1 figure and 3 tables

Received June 6, 2013/Accepted November 23, 2013Communicated by R. Varshney

AbstractChickpea (Cicer arietinum L.) is cultivated mostly in the arid and semi-arid regions of the world. Climate change will bring new production sce-narios as the entire growing area in Indo–Pak subcontinent, major pro-ducing area of chickpea, is expected to undergo ecological change,warranting strategic planning for crop breeding and husbandry. Conven-tional breeding has produced several high-yielding chickpea genotypeswithout exploiting its potential yield owing to a number of constraints.Among these, abiotic stresses include drought, salinity, water logging,high temperature and chilling frequently limit growth and productivity ofchickpea. The genetic complexity of these abiotic stresses and lack ofproper screening techniques and phenotyping techniques and genotype-by-environment interaction have further jeopardized the breeding pro-gramme of chickpea. Therefore, considering all dispiriting aspects of abi-otic stresses, the scientists have to understand the knowledge gapinvolving the physiological, biochemical and molecular complex networkof abiotic stresses mechanism. Above all emerging ‘omics’ approacheswill lead the breeders to mine the ‘treasuring genes’ from wild donorsand tailor a genotype harbouring ‘climate resilient’ genes to mitigate thechallenges in chickpea production.

Key words: Chickpea breeding — cold stress — droughttolerance — salinity stress — QTLs

Globally, chickpea (Cicer arietinum L.) is the second mostimportant legume crop after dry beans (Varshney et al. 2013b).According to FAOSTAT data (2012), chickpea is grown in 54countries with nearly 90% of its area covered in developing coun-tries (Gaur et al. 2012). Notably, almost 80% of global chickpeais produced in Southern and South-Eastern Asia and India ranksfirst in the world, contributing 68% of the global chickpea pro-duction accompanied by Australia (60%), Turkey (47%), Myan-mar (42%) and Ethiopia (35%) (FAOSTAT 2012, Gaur et al.2012). Worldwide chickpea production is estimated to be11.30 million tons from 12.14 million ha area with an averageproductivity of 931 kg/ha (FAOSTAT 2012). In India, it tops thelist of pulse crops and is cultivated in 8.32 million ha, producinga total of 7.70 million tons with an average yield of 925.5 kg/ha(FAOSTAT 2012). From the nutrition perspective, chickpea seedcontains 20–30% crude protein, 40% carbohydrate, and 3–6% oil(Gil et al. 1996). Besides, pulses supplemented diets are alsogood source of calcium, magnesium, potassium, phosphorus, ironand zinc (Ibrikci et al. 2003). Chickpea faces various abiotic

stresses during its life cycle such as drought, cold, terminal heatand salinity (Ryan 1997, Millan et al. 2006), and it also encoun-ters water logging, acidity and metal toxicity stresses. The yieldlosses due to abiotic stresses may exceed (6.4 million tons) thosecaused by biotic stresses (4.8 million tons) (Ryan 1997). Substan-tial economic losses of 1.3 billion, 186 million and 354 millionUS dollars due to drought/heat, cold and salinity, respectively,have raised tremendous concerns among the chickpea-growingcountries (Ryan 1997).Given the complex genetic architecture and unpredictable

occurrence, breeding against abiotic stresses has always been achallenging task. Further, drastic climate changes have causedphenotypic plasticity implying changes in phenotype of plant(Nicotra et al. 2010), and this phenotypic plasticity permits toadjust their form and function according to the change ofresource and habitat (Magyar et al. 2007). Tolerance to abioticstresses exhibits complex quantitative inheritance that is alsoinfluenced by a number of genetic and environmental interac-tions. As an obvious reason, these strong genotype-by-environ-ment (G 9 E) interactions have also posed impediments inbreeding against these stresses. An exhaustive search of germ-plasm for appropriate donors to these stresses represents the fore-most step in breeding for stress tolerance. Given the context, adetailed list of the genotypes showing tolerance to various abi-otic stresses has been presented in Table 1, which can be usedas potent resistant/tolerant sources for introgressing the quantita-tive trait loci (QTLs) governing stress tolerance to susceptiblevarieties. This review article summarizes the negative impactsand constraints of major abiotic stresses on chickpea yield alongwith providing a critical appraisal of various conventional breed-ing strategies. Additionally, this article also provides an over-view on recent developments of genomic resources and variousmolecular breeding (MB) approaches including marker-assistedbackcrossing (MABC), marker-assisted recurrent selection(MARS), which may act as powerful supplement to conventionalbreeding particularly in the context of abiotic stresses.

Drought StressBackground constraints and its effects

Drought is one of the most important abiotic stresses, which limitsproduction in different parts of the world and has remained the

Plant Breeding 133, 163–178 (2014) doi:10.1111/pbr.12150© 2014 Blackwell Verlag GmbH

Table 1: Sources of resistance to various abiotic stresses and their basis of tolerance in chickpea

Abioticstress Tolerant sources

Underlying mechanism/physiologicaland biochemical basis for tolerance References

Droughttolerance

H208, H355, S26, G24, RS10, RS11 and Azerbaijan 583 – Saxena and Singh (1987)ICC4958 Deep rooting, 30% more root volume

and mass than cultivated genotypesSaxena et al. (1993),Krishnamurthy et al.(2003) and Kashiwagiet al. (2005, 2006a)

FLIP 87-59C – Singh et al. (1996)ICC96029 Early flowering Kumar and Rao (1996)FLIP92-154C – Toker and Cagirgan (1998)ICCV2 Early flowering Kumar and Abbo (2001)ICCV93032, ICCV94008, ICCV90033 and ICC89204 – Kanouni et al. (2002)ICC5680, ICC10448 Small leaf and leaf area Saxena (2003)RILs from ICC4958 9 Annegiri Prolific rooting and deep rooting trait Serraj et al. (2004a)ILC1799, ILC3832, FLIP98-141, ILC3182, FLIP98-142C,ILC3101 and ILC588

Escape through earliness Sabaghpour et al. (2006)

ICC8261 Avoidance through root traits Gaur et al. (2008)Beja and Kesseb Lower nodule mortality Labidi et al. (2009)ICC4958, ICC8261 Root length density and root dry

weightKashiwagi et al. (2008)

ACC316 and ACC317 Early flowering(escape mechanism) Canci and Toker (2009)ICC13124 Root length, root weight and root

volumeParmeshwarappa et al.(2010)

HC-5 and H02-36 Rooting depth and root biomass Kumar et al. (2010a)MCC544, MCC696 and MCC693 Mesophyll resistance and proline

accumulationMafekheri et al. (2010)

ILC482 Higher proline content Mafakheri et al. (2011)ICC7571 Harvest index and rate of partitioning

positively associated with (DRI)Kashiwagi et al. (2013)

TerminalHeatstress

ILC482, Annegiri, ICCV10 Cell membrane stability Srinivasan et al. (1996)ICCV88512 and ICCV88513 – Dua (2001)ACC316and ACC317 Early flowering Canci and Toker (2009)ICC1205 Pollen germination and tube growth Devasirvatham et al. (2010)ICC456, ICC637, ICC1205, ICC3362, ICC3761, ICC4495,ICC4958, ICC4991, ICC6279, ICC6874, ICC7441, ICC8950,ICC11944, ICC12155, ICC14402, ICC14778, ICC14815,ICC15618

Early flowering, seed yield at maturity Krishnamurthy et al. (2011)

ICC14346 Early maturing Upadhyaya et al. (2011)ICCV92944 Early maturity Gaur et al. (2012)ICC1205 and ICC15614 High pod no; filled pods/plant under

heat stressDevasirvatham et al.(2012, 2013)

ICC14778 High rate of partitioning, cooler canopytemp. Extract maximum soil water

Kashiwagi et al. (2008),Zaman-Allah et al.(2011a,b) andKrishnamurthy et al.(2013a)

Freezingtolerance

Azerbaijan, ILC482 – Saxena and Singh (1987)ILC-794, ILC-1071, ILC1251, ILC1256, ILC1444, ILC1455,ILC1464, ILC1875, ILC3465, ILC3598, ILC3746, ILC3747

– Singh et al. (1989)

ILC3791, ILC3857, ILC3861, FLIP-85-81C, FLIP82-85C,82-313C, 84-112C, FLIP85-4C, FLIP 85-49C, FLIP 81-293C,FLIP 82-127C and FLIP82-128C

– Wery (1990)

ICCV 88502, ICCV88503 Pod set at cold temperature(tolerance/resistance)

Srinivasan et al. (1998,1999)

ICCV96029, ICCV96030 Earliness(escape mechanism) Sandhu et al. (2002) andKumar and Rao (1996)

ICCV88516 – Clarke and Siddique (2003)Sonali and Rupali Pollen selection at low temperature Clarke et al. (2004)MCC426 and MCC252 – Nezami et al. (2007)L550 Physiological Lauter and Munns 1986

Salinitytolerance

ICCC32 and 1CCL86446 – Dua (1992)CSG88101, CSG8927 Lower Na+ in root, that is, exclusion

of Na+Dua and Sharma (1995)

Amdoun l Protection of photosynthetic organfrom attack of Na+ by retaining Na+in root and supply of K+ to shoot

Slemi et al. (2001)

FLIP.98-74, FLIP.87-59, FLIP.87-85, and ILC 3279 Physiological Bruggeman et al. (2003)SG-11 and DHG-84-11 Physiological Singh et al. (2001) and

Singh (2004)CSG8962 and ICCV96836 – Maliro et al. (2004)CSG9651 – Singla and Garg (2005)ILC1919 Physiological Tejera et al. (2006)CM88 Biochemical Sarwar et al. (2006)ICC5003, ICC15610 and ICC1431 Higher yield under salinity Vadez et al. (2007)Hahshem – Sohrabi et al. (2008)JG62 Higher yield under salinity, Early

floweringVadez et al. (2007, 2012b)

164 U. C. JHA , S . K. CHATURVED I , A . BOHRA e t a l .

most recalcitrant when attempted to address through traditionalbreeding approaches (Tuberosa and Salvi 2006, Toker et al.2007a). It is important to note that the water scarcity alone causes70% of agricultural yield loss across the globe (Boyer 1982).Moreover, in concern with drought, desiccation has been reportedas the most severe form of drought that leads to loss of protoplas-mic water (Yordanov et al. 2003). Drought imposes negativeeffects on plant growth and development by impeding lipid bio-synthesis and lowering the membrane lipid, which ultimatelyresults in loss of membrane integrity (Pham-Thi et al. 1987,Monteiro de Paula et al. 1990, Gigon et al. 2004, Harb et al.2010) and irreversible cell damage (Vieira da Silva et al. 1974).Further, the water deficit hinders the foremost biological processof photosynthesis and other metabolic activity of plant (Chaves1991, Chaves et al. 2003, 2009, Pinheiro and Chaves 2011). Nota-bly, almost 90% of chickpea is grown under rainfed conditions(Kumar and Abbo 2001) where terminal drought limits its produc-tivity (Toker et al. 2007a). The result of drought relies upon thewater-holding capacity, evapo-transpiration and need of water forcrop plants (Toker et al. 2007a). Drought accounts for 40–45%yield losses in chickpea across the globe (Ahmad et al. 2005).

Strategy for drought acclimationHarnessing genetic variability, genetic basis and breeding for droughttoleranceTo a large extent, success of any crop-improvement programme isdetermined by the quantum of exploitable genetic variation thatexits in the crop germplasm. Keeping the above in view, a largenumber of accessions have been routinely screened for varioustraits specifically to incorporate drought tolerance in chickpea. Forinstance, a preliminary study conducted during 1992 to 1995 atTel Hayda (northern Syria) using 4165 lines by establishing theproper screening and rating scale (1–9), and subsequently, a totalof 19 drought resistant lines were identified (Singh et al. 1997). Ina similar manner, 64 chickpea lines were evaluated under rainfedconditions for drought tolerance showed 53% yield advantage ofthe mentioned lines under non-stressed conditions compared withstress conditions (Toker and Cagirgan 1998). Likewise, a set of 24genotypes was screened considering five important indices, viz.drought response index (DRI), stress tolerance index (STI), toler-ance (TOL), mean productivity (MP) and geometric mean produc-tivity (GMP), which were recorded under two different moisturelevels at two different sowing times. STI and MP were chosen asthe best indices for evaluation of drought resistance (Kanouniet al. 2002), and similarly, Pouresmael et al. (2013) reported STIas an important parameter for drought tolerance in chickpea.In any crop species, wild species are the natural reservoir of

both biotic and abiotic stress resistance. However, during theprocess of crop domestication and selection, these natural reser-voirs of immense genetic variation have gone unnoticed (Zamir2001). In regard to chickpea, perennial wild Cicer species, viz.C. anatolicum, C. microphyllum, C. montbretti, C. oxydon andC. songaricum, were evaluated for drought tolerance, using ascale of 1 (highly tolerant) to 5 (highly susceptible) (Toker et al.2007b). Taken into consideration the drought tolerance index(DTI), a mini-core collection comprising 211 chickpea acces-sions was screened for three consecutive years. The studyrevealed a wide range of variation for days to 50% flowering,maturity, shoot biomass and seed yield under drought condition,and the cluster analysis categorized five accessions as highly tol-erant, 78 as tolerant, 74 as moderately tolerant, 39 as sensitiveand 20 as highly sensitive (Krishnamurty et al. 2010). Similarly

from mini-core collection, 10 accessions were identified showingdrought tolerance relying on drought susceptible index (DSI)and drought tolerant efficiency per cent (DTE%), tested during2006–2007. The genotype ICC13124 performed best among thegenotypes used and gave maximum yield under irrigated(1220 kg/ha) and rainfed condition (990 kg/ha) (Parmeshwarap-pa et al. 2010). In another instance, screening of 377 accessionsusing 1 (free from heat and drought stress) to 9 (susceptible toheat and drought) scale led to identification of two genotypesviz. ACC316 and ACC317 possessing resistance to drought andheat accompanying least impact of heat and drought on seedweight and having highest heritability (Canci and Toker 2009).To find out the associations of various drought-related traitswith DRI, a set of 21 drought-responsive genotypes was testedfor two consecutive years and the experimental results demon-strated the positive association of crop growth rate (CGR) withDRI, whereas water-use efficiency (WUE) showed a negativecorrelation with the DRI (Kashiwagi et al. 2013). Moreover, onechickpea landrace (ICC 7571) exhibited a noticeably tolerantreaction against drought across both years. Kashiwagi et al.2013 also reported the significant contribution of rate of parti-tioning or partitioning coefficient (p) towards grain yield underdrought conditions, and this observation was also confirmed inanother study conducted on a reference collection of chickpeacomprising 280 cultivated accessions (Krishnamurthy et al.2013a). Under terminal drought stress, path analysis performedin the reference collection of chickpea exhibited the positiveassociations of carbon isotope discrimination with harvest index(HI) (Krishnamurthy et al. 2013b). In addition to germplasmcollections, segregating populations derived from possible com-binations of four genotypes viz. ICCV 2, A1, ICC 4958 andICCV 10448 were tested for physiological traits impartingdrought tolerance. Of the six F2 populations evaluated, highestyield was obtained from progeny sharing ICCV4958 as one ofthe parent. The segregates obtained from A1 9 ICC 4958, ICCV2 9 ICC 4958 explained high seed yield, early and high rootmass (Mannur et al. 2009). Efforts were also carried out to findout the gene actions underlying drought tolerance using jointscaling test in the cross ‘Hashem’ (cultivar) 9 ICCV 96029,and the investigation elucidated the presence of additive 9 dom-inance = [j] gene action for grain yield, biological yield andproline content, whereas duplicate epistasis (additive 9 domi-nance = [j] and dominance 9 dominance = [l] gene action) wasobserved for number of pods/plant and number of seeds/pod(Farshadfar et al. 2008). Two important QTLs (Q3-1 and Q1-1)underlying drought tolerance (given in Table 2) were identifiedfrom population ILC 588 9 ILC 3279, and these QTLs werelocated on LG3 and LG1 (Rehman et al. 2011). More recently,a comprehensive molecular investigation targeting genetic dis-section of drought tolerance was carried out in chickpea (Varsh-ney et al. 2013a). Two mapping populations namely ICC4958 9 ICC 1882 and ICC 283 9 ICC 8261 were chosen forrigorous phenotypic screening using a variety of drought compo-nent traits, which were phenotyped across five different loca-tions in India. The phenotypic data along with the genotypicdata were subsequently analysed to discover QTLs associatedwith drought tolerance. Importantly, not only main-effect QTLs(45 m-QTLs) but epistatic-QTLs (e-QTLs) were also detectedindicating the occurrence of complex genetic interactions con-trolling drought tolerance. In total, the 45 m-QTLs explainedalmost 60% variance, while 973 e-QTLs accounted upto 90% ofthe phenotypic variance for various component traits (Varshneyet al. 2013c).

Stress breeding in chickpea 165

Physiological and biochemical toleranceThe plant acclimatizes under drought conditions through differ-ent mechanisms like escape, avoidance and tolerance (Levitt1972, Turner 1986, Loomis and Connor 1992). Drought resis-tance and its components are almost constantly being redefined(Blum 2005).

Drought escape through early phenologyDrought escape enables selection of plants completing their lifecycle in short period thus making judicious use of availablemoisture condition (Turner and Whan 1995, Siddique et al.1997). Under terminal drought conditions, early flowering traitprovides advantage of avoiding drought and avoids yield loss inchickpea (Subbarao et al. 1995, Siddique et al. 1999, Kumar andAbbo 2001, Berger 2007). In context of early flowering, a majorrecessive gene ‘efl-1’ was reported to be responsible for earlyflowering (Kumar and van Rheenen 2000), and this finding sub-sequently facilitated the development of super early genotypeICCV 96029 (derived from ICCV 2 9 ICCV 93929 cross)which flowered within 24 days (Kumar and Rao 1996) at ICRI-SAT. Sabaghpour et al. (2006) screened a total of 40 kabuligenotypes and identified ILC1799, ILC3832, FLIP98-141,ILC3182, FLIP98-142C, ILC3101 and ILC588 as superior earlygenotypes that can escape terminal drought (Table 1). However,selection of genotypes with shorter vegetative period may resultin yield penalty (Basu and Singh 2003).

Drougth avoidance through root traitsRoot system of plant imparts drought tolerance through acquiringsoil moisture by deep penetration of root, adequate root densityand sufficient longitudinal conductance of main roots (Fisheret al. 1982). Chickpea genotypes with high root biomass andshowing marked drought tolerance have been reported (Brownet al. 1989, Saxena et al. 1994, Krishnamurthy et al. 1996). Oneof such drought resistant genotype ICC4958 recorded 30%higher advantage in root dry matter as compared to ‘Annegiri’

(Saxena et al. 1994). Among various root traits, the depth ofrooting allows availing the deep soil water in drought conditions(Saxena et al. 1993, Krishnamurthy et al. 2003 and Kashiwagiet al. 2005). Role of deep and prolific rooting trait affectingdrought avoidance and yield was examined usingICC4958 9 ‘Annegiri’ based RIL population consisting of 257lines. However, no significant yield improvement was recordedin this study (Serraj et al. 2004a). In addition, the ‘root lengthdensity’ (RLD) and maximum ‘root depth’ (RDp) can benefit indrought resistance without affecting yield as assessed in mini-core collection of chickpea (Kashiwagi et al. 2005). Using 12chickpea genotypes, a positive association of RLD with seedyield was illustrated at 35 days after sowing (DAS) (Kashiwagiet al. 2006a). Notably, genotypes with prolific and deep rootinghave been found to be more adapted to drought, but little infor-mation is available on the genetic control of root system. Takenthe above into account, generation mean analysis (GMA) wasconducted to estimate the genetic effects of root and shoot traitsusing six generations (P1, P2, F1, F2, BC1P1 and BC1P2) basedon two different crosses viz. ICC283 9 ICC 8261 andICC4958 9 ICC1882. The study suggested existence of additivegene action and additive 9 additive gene interactions, whichcontrol RLD and root dry weight (RDW) (Kashiwagi et al.2008). In contrast to the destructive method involved in screen-ing of root traits, polyvinyl chloride (PVC) pipes are used mak-ing the sampling of root traits easier and efficient in chickpea(Upadhyaya et al. 2012). In an investigation aiming at detectingsignificant QTLs, a major QTL was discovered that controlledone-third of the entire variation for root length and root biomass(Chandra et al. 2004). Kumar et al. (2010a) investigated the roottraits for drought tolerance in six genotypes in both irrigated andrainfed conditions and identified two genotypes viz. HC-5 andH02-36 showing high dry matter of roots, high root depth,and high root to shoot ratio, and ultimately, the plant yieldadvantage. However, it has also been observed in some recentstudies that profuse and deep rooting do not contribute drought

Table 2: Different QTLs identified for various abiotic stresses in Chickpea

Trait Mapping population Markers Identified QTLLinkagegroup

Phenotypicvariation (%) References

Droughttolerance/avoidance

ICC4958 9 Annigeri – One major QTL contributingroot biomass

– – Gaur et al. (2008)

ICC8261 9 ICC283 and QTLs contributing root traits – – Gaur et al. (2008)Droughttolerance

ILC 588 9 ILC 3279 97 SSRmarkers

Two QTL for HI – 38 Rehman et al. (2011)

– Four QTL for flowering – 45 Rehman et al. (2011)– Three QTL for maturity

explaining– 52 Rehman et al. (2011)

– Three QTL for gs +six QTLfor Tc–Ta

– 7–15 Rehman et al. (2011)

– Two QTL (Q3-1 and Q1-1) LG3 andLG1

– Rehman et al. (2011)

Droughttolerance

ICC4958 9 Annigeri TAA170,ICCM0249,STMS11and GA24

Several QTLs contributingdrought tolerance

LG4 – Jaganathan et al. (2013)

Salinitytolerance

ICCV 2 9 JG 62 216 markers One QTL for seed yield undersalinity on

LG3 19 Vadez et al. (2012a)

ICCV 2 9 JG 62 – Many QTL associated withseed no and 100 seed wtunder salinity

LG 6 14.8–49.7 Vadez et al. (2012a)

ICCV 2 9 JG 62 – Many QTL associated with50% flowering, seed no.shoot dry wt.

LG 4 8.8–37.7 Vadez et al. (2012a)

gs, Higher stomatal conductance; [Tc–Ta], cooler canopies (canopy temperature minus air temperature); HI, Harvest Index.


tolerance in terms of improving yield under drought stress,whereas some moisture preservation traits determine yieldimprovement under drought in chickpea (Zaman-Allah et al.2011a,b).

Tolerance through osmotic adjustmentOsmotic adjustment (OA) is an important physiological phenom-enon, which controls the water absorption and cell turgor pres-sure under drought stress (Cattivelli et al. 2008). OA confersdrought tolerance in many crops of commercial importance likewheat (Blum et al. 1999, Morgan 2000), barley (Blum 1989),sorghum (Morgan 1984). In addition to sustaining turgor mainte-nance during water stress condition (Ali et al. 1999), OA alsoplays a significant role during grain formation under droughtstress in wheat (Morgan and Condon 1986). Similarly, severalreports have been published in chickpea providing knowledgeabout the association of OA and yield (Morgan et al. 1991, Basuand Singh 2003, Moinuddin and Khanna-Chopra 2004). Forexample, Serraj and Sinclair (2002) deduced positive role of OAin regard to yield through root development towards higher soilwater. However, no strong evidence was reported concerning thedirect association of OA with yield of plant under drought stress.With the progress of water stress, OA enhances progressivelywitnessed by measuring plant water potential and relative watercontent (RWC) (Lecoeur et al. 1992). By subjecting a set ofadvanced breeding lines of chickpea to drought stress, variationin OA was recorded for both Indian and Australian conditions.No yield advantage was seen under Australian conditions, exceptthe case of early flowering where OA effect exhibited high yieldadvantage (Turner et al. 2007). Similarly, Basu et al. (2007) alsoinvestigated the genetic difference for OA existing among differ-ent chickpea genotypes. They also suggested that lowering waterpotential will reduce the leaf starch content, but soluble sugarshexoses and sucroses get increased, not due to change in OA,suggesting reliability of OA for drought tolerance is not promis-ing in chickpea.Water-use efficiency (WUE) is described as amount of bio-

mass produced at the cost of per unit transpired water (Bacon2004). High WUE is another important criterion while dealingwith drought tolerance, and it is calculated by graviometricmethod in pot culture based on transpiration and yield correla-tion (Krishnamurthy et al. 2007, Upadhyaya et al. 2012).A robust screening technique known as carbon isotope discrimi-nation (D13C) was used for measuring WUE in chickpea (Kash-iwagi et al. 2006b). At different levels of vapour pressuredeficit under both field and controlled conditions, some chick-pea genotypes displayed low canopy conductance especially atvegetative stage under irrigated conditions and exactly oppositeat pod filling stage (Zaman-Allah et al. 2011a,b). Based onnodule mortality symptom, inoculating five lines with Mesorhiz-obium ciceri UPMCa7 and noticing change in N content androot to shoot ratio, loss of chlorophyll, and consequently, thegenotypes ‘Beja’ and ‘Kesseb’ were found to be tolerant underdrought conditions (Labidi et al. 2009). Similarly, antioxidantenzyme activities of ascorbate peroxidase and peroxidase innodule produced by Mesorhizobium ciceri strains contribute todrought tolerance in chickpea (Esfahani and Mostajeran 2011).By imposing drought at three different growth stages viz. (i)vegetative, (ii) anthesis and (iii) both the vegetative and anthe-sis stage, more accumulation of carbohydrate, catalase (CAT)and peroxidase (POX) was observed in tolerant genotypes indi-cating the importance of CAT and POX in drought tolerance

(Mafakheri et al. 2011). With the purpose of identifying somenew resistant sources to breed for drought tolerance, the toler-ance or susceptibility reactions of 150 Iranian kabuli genotypeswere checked under rainfed and irrigated conditions. The resultsobtained were further validated using a pot experiments, and asa consequence, three genotypes MCC544, MCC696 andMCC693 were declared as tolerant to drought stress (Ganjealiet al. 2011). The above investigation also confirmed the pre-sence of significant negative correlations between yield anddays to flowering under drought conditions. Moreover, it alsoprovided emphasis on the fact leaf area can be taken as a deci-sive factor, while assessing the drought tolerance due to lesstranspiration in decreased leaf area. While evaluating 14 chick-pea accessions under moisture and non-moisture environment,three genotypes namely Phule G09103, Phule G 2008-74 andDigvijay were found as drought tolerant which may be due tohigher value of drought tolerance efficiency, chlorophyll con-tent, proline content, reduction in drought susceptibility andmembrane injury indices (Ulemale et al. 2013). Other crucialphysiological parameters viz., photochemical efficiency of PIIsystem, RWC, SPAD chlorophyll metre reading, cell membraneintegrity and stomatal conductance contributing to drought toler-ance have also been investigated in chickpea (Pouresmael et al.2013).

Terminal Heat StressBackground constraints and its effects

Concerning heat stress, Wahid et al. (2007) reported that the risein temperature beyond certain optimum level is detrimental tothe crop growth causing severe injuries that are collectivelytermed as ‘heat stress’. Impact of high temperature on plantgrowth has been reported on various legume crops including drybean (Prasad et al. 2002), groundnut (Prasad et al. 2003) andsoybean (Baker et al. 1989). However, a significant progress hasnot been achieved in regard to the effect of heat on differentmorphological and physiological stages of chickpea (Wang et al.2006). Being a cool season crop, chickpea is also susceptible tohigh temperature (30–35°) for few days at flowering stage andcan cause substantial yield loss (Summerfield and Wein 1980,Saxena et al. 1988). Summerfield et al. (1984) found the nega-tive relationship between the effect of high temperature at repro-ductive phase and yield in chickpea. Evolution or more preciselythe domestication of chickpea has enforced the selection of vari-ous phenological changes in accordance with the changes ofhabitats (Berger et al. 2011). In the Mediterranean region, chick-pea confronts extremely low temperature in winter (Berger 2007)and tremendously high temperature during the reproductive stage(Iliadis 1990). While in case of Indian subcontinent condition,chickpea encounters day temperature of 5–10°C during vegeta-tive stage and 20–27°C and even >30°C temperature duringreproductive stage (Summerfield et al. 1984, 1990, Berger andTurner 2007). Exposure of various chickpea genotypes beyond35°C temperature shows no pod setting (Basu et al. 2009). Thepreanthesis and anthesis stages are the stages that are most vul-nerable to high temperature stress (Devasirvatham et al. 2013).High temperature hampers photosynthesis by damaging bothstructural and functional activity of chlorophyll and lowers thechlorophyll content (Xu et al. 1995). Temperature beyond 40°Ccauses disruption in photo system I and II (Baker 1991, Sharkey2005) and also affects respiration (Kurets and Popov 1988),membrane composition and its stability (Levitt 1969), nitrogen


fixation (Black et al. 1978) and water relation (McDonald andPaulsen 1997). High temperature stress exerts pronounced effecton reproductive phase, which leads to impairment in pre-anthe-sis, postanthesis and fertilization processes ultimately resulting inloss of seed weight and yield (Nakano et al. 1997, 1998, Prasadet al. 2003, Upadhyaya et al. 2011). In chickpea, high tempera-ture stress also causes reduction in number of flowers, pollenproduction, pods/plant and most importantly, the filled pods/plant (Wang et al. 2006, Basu et al. 2009, Devasirvatham et al.2012). The sensitivity of chickpea pollen to high temperature ismore than stigma, and this observation has been confirmed bothin field as well as under controlled conditions using genotypeslike ICC1205/ICC15614 (heat tolerant) and ICC 4567/ICC10685(sensitive) (Devasirvatham et al. 2012, 2013). Heat stress marksnoticeable effects in anther locule number, anther epidermis wallthickening and pollen sterility (Devasirvatham et al. 2013). Forinstance, when ICC 5912 was kept at 35/20°C for 24 h beforeanthesis, the genotype became sterile, whereas the other geno-type ICCV92944 produced fertile pollens (Devasirvatham et al.2010).

Strategy for heat acclimationHarnessing genetic variability, genetic basis and breeding for heat tol-eranceGermplasm variability for heat tolerance is inevitable for devel-oping a genotype with heat tolerance. Dua (2001) documentedtwo genotypes ICCV 88512 and ICCV 88513 exhibiting heattolerance. Another chickpea genotype ICCV 92944 was declaredas heat tolerant in field condition (Gaur et al. 2010) and subse-quently released as cultivar in India (JG14) and Myanmar (Yezin6) (Gaur et al. 2012). Furthermore, while screening the referencecollection (280 accessions) at two locations in India (Patancheruand Kanpur), three genotypes ICC3362, ICC6874 and ICC12155were shown as heat tolerant based on the criterion ‘heat toler-ance index’ (HTI) (Krishnamurthy et al. 2011). Similarly, apromising heat-tolerant line ‘ICC14346’ was recovered throughthe assessment of 35 different early maturing germplasm lines(Upadhyaya et al. 2011). Likewise, taken the pod setting ability(under high temperature ≥37°C) into consideration, Devasirva-tham et al. (2012, 2013) registered two chickpea genotypesICC1205 and ICC15614 as heat-tolerant lines. Notwithstandingthe immense importance of heat tolerance, extensive studies havenot been carried out to discover the inheritance patterns of heattolerance in chickpea. However, recently Upadhyaya et al.(2011) suggested that heat tolerance in chickpea is under thecontrol of multigenes. As an alternative to direct selection of theheat-tolerant genotypes, choice of early flowering and maturitygenotypes can be made, thereby bypassing cumbersome pheno-typing for heat stress in Mediterranean spring sown and southIndian sown chickpea (Toker et al. 2007a, Berger et al. 2011).While understanding the mechanism of heat tolerance, cell

membrane stability can be chosen as an important index (Sulli-van 1972), which is evident from various reports availablefrom different legumes including chickpea (Srinivasan et al.1996). Other factors like lipid composition and heat shock pro-tein accumulation in the pollen can also assist in identificationof heat-tolerant genotypes (Blum 1988). Besides, osmoregulatorcontents can also provide defiance against heat stress (Evanand Malmberg 1989, Flores 1991). Importantly, the externalapplication of abscisic acid (ABA) can protect plant from heatstress by inducing other osmolytes viz., proline, glycine betaineand trehalose (Kumar et al. 2012). Electrolyte leakage and fluo-

rescence tests can aid in screening for heat stress (Srinivasanet al. 1996). Additionally, as reported in some cereal crops likewheat, high grain filling rate and high grain weight under heatstress condition can also act as crucial selection criteria for heattolerance (Tyagi et al. 2003, Singha et al. 2006, Dias and Li-don 2009). Similarly, in case of chickpea, pod filling rate andhigh 100-seed weight can be important selection parameters forheat tolerance. Nevertheless, Fokar et al. (1998) suggestedsome other important standards to assess heat tolerance likestay green character and retention of chlorophyll under heatstress. In the current scenario of rising global temperature,screening of pollen viability and pollen-based screening tech-niques under high temperature can be particularly beneficial forelevating the levels of heat tolerance in chickpea genotypes(Devasirvatham et al. 2012).

Low Temperature StressBackground constraints and its effects

Cold temperature stress represents a major limiting factor inchickpea production especially in North India, Canada and someparts of Australia. Based on the severity of cold, low tempera-ture injury can be classified into two types: (i) chilling injurywhen temperature remains above freezing point (>0°C) and(ii) freezing injury at temperature below freezing point (0°C).The chilling and freezing injury cause serious damages to plants,which includes disruption of membrane (Steponkus et al. 1993,McKersie and Bowley 1997), hampered pollen formation or pol-len germination. Moreover, it adversely affects photosynthesis(Bell 1993), electron transport (Hallgren and Oquest 1990) andenzymes involved in CO2 fixation (Sassenrath et al. 1990). Dueto chilling temperature, the activities of reactive oxygen species(ROS) increase and thus, aggravate chilling injury (Omran 1980,Hodgson and Raison 1991, Prasad et al. 1994). Cold tolerancemechanism involves a series of biochemical and physiologicalchanges that cause increase in ABA (Rikin and Richmond 1976,Ciardi et al. 1997, Morgan and Drew 1997), alteration in lipidcomposition in cell membrane (Graham and Patterson 1982, Mu-rata 1983, Tasaka et al. 1990) and also the changes in osmolytesand increase in antioxidants (Fridovich 1986, Halliwell and Gut-teridge 1989). Low temperature stress is becoming more preva-lent in temperate region creating a serious threat to vegetativegrowth by several means like creating chlorosis, necrosis of leaftip and curling of whole leaf. Similarly, reproductive stage repre-sents the most vulnerable phase within where plenty of damag-ing events may take place, such as, the juvenile buds drop,aborted pods, reduced pollen viability and stigma receptivity,inhibited pollen tube growth and ultimately, deteriorated seedquality and seed yield (Kumar et al. 2007, 2010b). The harmfuleffect of low temperature (below 15°C) is reported from variouschickpea-growing areas like Australia (Siddique and Sedgley1986), Mediterranean region (Singh 1993), India (Savithri et al.1980, Srinivasan et al. 1998) and even within controlled labora-tory conditions (Srinivasan et al. 1999, Clarke et al. 2004, Nay-yar et al. 2005).

Strategy for low temperature tolerance acclimationHarnessing genetic variability, genetic basis and breeding for low tem-perature toleranceIdentification of cold tolerant chickpea in Mediterranean regionposes the essential prerequisite for enhancing yield during wintersowing, both at freezing (below �1.5°C) and chilling (�1.5 to


15°C) temperatures, which affects the entire crop developmentprocess starting from germination to maturity (Croser et al.2003). Phenological stage should be taken under considerationfor assessing the cold tolerance of a genotype from germinationto flowering stage. To ascertain the sowing date for freezingresistance, 29 genotypes were screened at five locations at twosevere winter (�10°C to �18°C) temperatures, as a result FLIP81-293C, FLIP 82-127C and FLIP82-128C offered resistance tolow temperatures (Wery 1990). In regard to the number of genesunderlying tolerance, the genetics of cold tolerance was eluci-dated by Malhotra and Singh (1991). They considered six differ-ent crosses for applying combining ability and GMA, andconsequently, the presence of additive 9 additive and domi-nance 9 dominance interactions with duplicate epitasis wasrevealed. Furthermore, the inheritance analysis also demonstratedthat tolerance to cold is dominant over susceptibility.Considering pollen as vital component in manipulating the

chilling tolerance, selections for pollen at gametophytic stagepracticed in chickpea and flower colour was chosen as an effec-tive visible marker during the selection of genotypes (Clarkeet al. 2004) Alternatively, mutation breeding has also appearedas promising way to creating freezing stress tolerant genotypesin chickpea (Akhar et al. 2011). Use of gamma rays as a potentmutagen to induce mutation was manifested in three chickpeagenotypes at different doses, that is, 60, 100, 140 and 180 Gy ofgamma rays and keeping the shoots at LT50 (50% of lethal tem-perature). The two genotypes MCC741 and MCC495 showedthe highest survival of 80.1% and 64.6% at 180 and 140 Gydoses, respectively (Akhar et al. 2011). With the objective ofdeveloping high yielding and low temperature tolerance in coolerregion, a panel of 40 genotypes with a susceptible check ILC533was tested considering different phenological and postharvesttrait data for assessing cold tolerance. The genotypes showinghigh tolerance to cold were FLIP95-255C, FLIP93-260C andSel95TH1716 (Kanouni et al. 2009). As another notable obser-vation, morphological traits such as plant height, number of pri-mary branches and number of leaves were found to be more incold tolerant chickpea genotypes in comparison with sensitivegenotypes especially at early stage (30 and 60 DAS) (Chohanand Raina 2011). Annual wild species of chickpea have thepotential for freezing tolerance as evident from three C. echino-spermum and two C. reticulatum annual wild chickpea geno-types along with 225 cultivated genotypes of chickpea in bothfield and controlled condition. The most promising wild acces-sions were ILWC81, ILWC106, ILWC139, ILWC181 andILWC235, whereas cultivated genotypes exhibiting tolerancewere Sel96TH11404, Sel96TH11439, Sel96TH11488,Sel98TH11518, x03TH21 and FLIP93-261C (Saeed et al. 2010).Besides lines of C. bijugum, ILWC-29/S-10 line of C. pinnatifi-dum and ILWC-35/S-3 line of C. echinospermum were reportedas resources of freezing tolerance (Singh et al. 1990).

Physiological and biochemical basis of toleranceAs indicated by double bond index (DBI), the external applica-tion of abscisic acid (ABA) increases fatty acid desaturation inplasma membrane and results in low cell lysis at low temperature(Bakht et al. 2006). Cold stress can be ameliorated by glycinebetaine application at budding stage, which improves pollen ger-mination, pollen viability, pollen tube growth, stigma receptivityand ovule viability. On the other hand, application at poddingstage increases seed yield, number of seeds/pod and RWC (Nay-yar et al. 2005). The fundamental changes by which external

ABA confers cold tolerance in chickpea involve retention ofchlorophyll, greater pollen viability, pollen germination, flowerretention and pod set, increase in seed weight and single seededpod, and decrease in infertile pod in comparison with coldstressed plants. Further, ABA also prevents the oxidative damagethrough enhancing the activities of antioxidants and proline inplant (Kumar et al. 2007). Similarly, Bakht et al. (2006), illus-trated application of exogenous ABA aids in acclimation in frostcondition. It has also been reported that antioxidative enzymessuch as catalase, ascorbate peroxidise, glutathione reductase andsucrose synthase can protect seeds and pod walls from the coldstress and thus can help greatly in developing cold tolerant linesin chickpea (Kaur et al. 2009).

Salt StressBackground constraints and effects

Chickpea production is adversely affected due to salinity in aridand semi-arid regions of world (Ryan 1997, Ali et al. 2002).Dua (1992) determined the threshold level of electrical conduc-tivity (EC) of 6dS for survival of chickpea under salinity. Saltstress (i) reduces water potential (Hayashi and Murata 1998,Munns 2002, Benlloch-Gonzalez et al. 2005), (ii) creates imbal-ance in ion (Hassanein 2000) and (iii) causes toxicity. Salinityalso imposes osmotic stress and ion toxicity (Munns 2005), ion-imbalance and nutrient deficiency (Tejera et al. 2006) in plant.Millan et al. (2006) discussed the effects of soil salinity onanthocyanin pigmentation in foliages of both desi and kabulitypes chickpea. In addition to inhibiting growth, photosynthesis,energy and lipid metabolism (Ramoliya et al. 2004, Parida andDas 2005), salinity also restrains flower and pod formation (Kat-erji et al. 2001, Vadez et al. 2007, 2012a). Sohrabi et al. (2008)analysed the effect of sodium (Na) salinity at different levels (0,3, 6 and 9dSm-1) in kabuli (‘Hashem’ and ‘Jam’) and desi(‘Kaka’ and ‘Pirooz’) genotypes for growth and yield parametersuggested the plant growth, pod number, flower, seed weightand seed number get reduced due to the effect of salinity. More-over, salinity also exerts negative effects on nodulation, nodulesize and N2 fixation (Swaraj and Bishnoi 1999, Flowers et al.2010). Interestingly, Samineni et al. (2011) declared that bothgrowth stages, that is, vegetative and reproductive are equallysensitive to salinity.

Strategy for salinity acclimation

Like other breeding programmes, breeding for salt tolerancerelies on assessment of allelic variation for salt tolerance in thegermplasm accompanied by transferring the beneficial allele(s)/gene(s)/QTLs to the other genetic background to create modernhigh-yielding cultivars.

Harnessing genetic variability, genetic basis and breeding for salinitytoleranceGenetic variation in chickpea genotypes for yield under salinestress was evaluated by several researchers (Sharma et al. 1982,Saxena 1984, Flowers et al. 2010). Assessment of 160 genotypesof chickpea using 50 mM NaCl or 25 mM Na2So4 salt facilitatedidentification of the salt tolerant cultivar ‘L550’ and showed thatthe presence of Na in the shoots checked the normal growth ofplant under salinity stress (Lauter and Munns 1986). In anotherinstance, the tolerance of two chickpea genotypes ICCC32 and1CCL86446 against chloride ion Cl- salinity was demonstrated


choosing various yield parameters (Dua 1992). The same way,effects of salinity were tested at germination and seedling stagesin a set of 30 chickpea genotypes. The genotypes C10, C14,C16, C17, C19 and C29 had tolerance for medium salinity(6 dS/m). Notably, the two genotypes C28 and C29 retainedtheir tolerance at all salt levels (Al-Mutawa 2003). Likewise,imposing salinity of 0.5, 2, 4, 6 dS/m in six genotypes resultedin comparatively higher production of dry matter by the geno-types FLIP97-74, FLIP87-59 and ILC3279 (Bruggeman et al.2003). Of 252 accessions, 211 mini-core collections of chickpeawere examined for salt tolerance, and kabuli types exhibited tol-erance to salinity, whereas desi types had susceptibility to salttolerance (Serraj et al. 2004b). Extensive genetic variability forsalinity was observed in 200 accessions of chickpea including19 wild relatives (Maliro et al., 2004). In a similar manner, largedegree of variation was also evident in 263 accessions of chick-pea mini-core collection, and a positive relationship (r2 = 0.5)was found between seed yields obtained under salinity and non-salinity conditions. The report also suggested that the desi typesare more tolerant than kabuli types (Vadez et al. 2007). A QTLanalysis conducted on population ICCV 2 9 JG 62 revealedoccurrence of significant QTLs for seed yield under saline condi-tion and these QTLs were mapped on linkage group 6 (Vadezet al. 2012b). An exhaustive testing for salt tolerance was per-formed on a sample consisting of landraces and wild relativesfrom 28 different countries using three different sampling strate-gies based on scoring of necrosis score and shoot biomass reduc-tion (Maliro et al. 2008). Considerable genetic variation forsalinity tolerance was noticed among 55 chickpea genotypes thatwere tested at variable salinity levels, and it was concluded thathigh pod and seed number bearing genotype which gathers lowconcentration of salt will provide better tolerance under salinitystress in chickpea (Turner et al. 2013). While practicing selec-tion, emphasis should be placed in the direction of constitutive(higher number of flowers) and adaptive traits (higher number ofseeds) for salinity tolerance in chickpea (Vadez et al. 2012a).

Physiological and biochemical basis of toleranceSeveral physiological parameters such as stomatal conductance,evapo-transpiration and leaf area, and essentially, yield can bechosen as factors for determining the tolerance against salinity(Katerji et al. 2003). Another important physiological parametersviz., early maturity, higher predawn water potential, maintenanceof high osmotic adjustment and retention of high number ofstems per plant can provide tolerance to salinity (Katerji et al.2005). The negative effect of salinity on plant growth was inves-tigated by Singla and Garg (2005), using two desi (CSG8962and DCP92-3) and two kabuli (CSG9651 and BG267) testedunder different salinity levels of 0, 4, 6 and 8/dSm resultingreduction in dry matter of root and shoot and ultimately loweringin productivity. CSG9651 performed high tolerance to salinity.Ion exclusion is a fundamental mechanism through which plantscan tolerate salt concentrations (Munnes and James 2003, Gart-hwaite et al. 2005), which was elucidated in chickpea by reten-tion of Na+ in root and supply of K+ to shoot in Amdoun 1(tolerant) and Chetoui (sensitive) (Slemi et al. 2001).

Water Logging StressExcess moisture and water logging predispose plants to diseaseattacks and insect pests that finally affect the yield and qualityof grains. Given the context, at flowering stage, water logging

causes mortality in chickpea ranging from 10% (line 946-512) to65% (cv. ‘Amethyst’) (Singh and Singh 2011). The mortality ofplants increased with water logging just before and after flower-ing of plant confirming 13% mortality of plants under water log-ging for 6 days before flowering. The mortality rates wererecorded as 65% and 100% with water logging one day afterflowering and 7.5 days after flowering, respectively (Cowieet al. 1995). Similarly, a set of 100 accessions was grown inexcess of water for 50 days, and based on experimental results,it was noticed that 19 genotypes did not show any germination,five genotypes survived upto <20 days. Outstandingly, the prog-eny derived from the cross DZ10-4 9 JG9-2-3-88 had toleranceand survived for 45–60 days (Bejiga and Anbessa 1995). Fur-ther, the effects of water logging at various physiological stageswere monitored by keeping the plants in waterlogged conditionshowed survival of plant decreases in water logging conditionwith increase in physiological stage (Cowie et al. 1996). Theeffect of water logging on root growth, plant biomass and seedyield was examined in two chickpea cultivars, ‘Almaz’ and ‘Ru-pali’ witnessing 54% and 44% yield reduction, respectively (Pal-ta et al. 2010).

Impact of Molecular Breeding and Genomics and ItsHope in Abiotic Stress Breeding in ChickpeaOwing to its quantitative inheritance, drought tolerance remainsa complex attribute, which is controlled not only by major-effectQTLs but also by plenty of such QTLs experiencing smallereffects on the phenotype (Varshney et al. 2013a). Additionally,the other phenomena like G 9 E and epistatic interactions alsohamper the progress of trait improvement using traditionalbreeding techniques (Varshney et al. 2013b). Therefore, tostrengthen the chickpea breeding, several genomic tools andtechnologies have been developed recently that have apparentlyenabled the detailed dissection of the complex traits (Varshneyet al. 2013a). A holistic approach enabling the implementationof the genomic tools and technologies, and the judicious exploi-tation of available genetic recourses for improvement of abioticstress has been illustrated in Fig. 1. Among various MBschemes, marker assisted backcrossing (MABC) is the simplestmethod routinely used for defect elimination (Hospital 2003,Varshney and Dubey 2009, Gupta et al. 2010). Technically, itresembles conventional backcrossing, and here, gene/QTLs aretransferred from donor parent to elite cultivars with the help ofmarker-based foreground and background selections therebyeliminating the chances for receiving the undesirable linkagedrags (Hospital and Charcosset 1997, Frisch et al. 1999).MABC is the method of choice to incorporate QTLs that controlsizeable variation for the trait of interest. Recently, MABC tech-nique was undertaken at ICRISAT to transfer drought tolerancefrom ICC 4958 to JG 11 and from ICC 8261 to two kabulichickpea cultivars ‘KAK 2’ and ‘Chefe’ (Gaur et al. 2012).With the similar objective of introgressing drought tolerance,extensive use of MABC was demonstrated successfully in trans-ferring a genomic region that harbours several QTLs related toroot and drought traits (described as QTL-hot spot) from ICC4958 to a popular high-yielding cultivar ‘JG11’ (Varshney et al.2013a). Besides MABC, other potential MB approaches likeMARS have also been propounded, which are able to tap thegenetic variation that is accounted to smaller effects QTLs(Varshney et al. 2013c). Nevertheless, in contrast to MABCwhich exploits pre-estimated QTL effects, MARS scheme


involves the construction of an ad hoc marker index, and this isfurther accompanied by marker index-based selections of desir-able genotypes and intercrossing of the selected individuals inadvanced generations (Stamp 1994, Ethington et al. 2007, Ri-baut and Ragot 2007, Bernardo 2008, Ribaut et al. 2010, Guptaet al. 2010, Tester and Langridge 2010, Chamarthi et al. 2011,Gaur et al. 2012). Experimental as well as simulation resultshave confirmed that the magnitude of genetic gains achievablethrough MARS scheme is more than the phenotypic selection(PS) and MABC (Bernardo and Charcosset 2006, Eathingtonet al. 2007, Ribaut and Ragot 2007, Gupta et al. 2010). By itsvirtue, MARS is efficient in extracting several minor-QTLs scat-tered throughout the genome (Ribaut and Ragot 2007, Varshneyet al. 2013b). Given the context, MARS was attempted recentlyin chickpea for transferring QTLs related to complex traits inchickpea (Gaur et al. 2012). QTLs attributing yield-related traits

under salinity (Vadez et al. 2012b) and drought (Rehman et al.2011) have been mapped recently (Table 2). Similar to MARS,advanced backcross QTL (AB-QTL) is another MB scheme thatdoes not need predefined gene-trait associations (Tanksley andNelson 1996). Given its ability to capture the tremendousgenetic variation existing among wild relatives, AB-QTLscheme has also been implemented in chickpea at ICRISAT(Gaur et al. 2012, Varshney et al. 2013d). Apart from MABCand MARS, another MB method has been invented, in whichgenotypes are selected on the basis of genome-wide markerinformation, and the method is known as genomic selection(GS) or genome-wide selection (GWS) (Meuwissen et al. 2001,Bernardo 2010, Varshney et al. 2013d). Instead of detecting sig-nificant QTLs, the DNA marker data and phenotyping scores inGS are used to calculate genomic estimated breeding value(GEBV), and GEBV is later used to select worthy individuals

Fig. 1: Deploying genomic tools and technologies in regular breeding for enhancement of abiotic stress tolerance

Table 3: Genomic resources for various abiotic stresses in chickpea

Trait ESTs/Transcript developed Technique used References

Drought tolerance 2800 ESTs Subtractive Suppressive hybridization (SSH) Jayashree et al. (2005)Drought tolerance 17 493 unique transcripts SuperSAGE Molina et al. (2008)Drought tolerance 20 162 ESTs cDNA libraries Varshney et al. (2009)Drought tolerance 319 unique ESTs Jain and

Chattopadhyay (2010)Drought tolerance 4815 differentially expressed unigenes DNA microarray Wang et al. (2012)Drought tolerance 3062 unigenes SSH Deokar et al. (2011)Drought tolerance 1278 genes regulated under drought 454/Roche GS FLX Titanium platform Jain et al. (2013)Salinity tolerance 21 401 unique transcript Next Generation Sequencing and super SAGE Molina et al. (2011)Salinity tolerance 1163 genes regulated under salinity 454/Roche GS FLX Titanium platform Jain et al. (2013)Drought, Cold andhigh salinitytolerance

215 and 30 genes, consensually differentiallyexpressed (DE) for susceptible and tolerantgenotypes for drought, cold and salinity

cDNA microarray approach Mantri et al. (2007)

Cold tolerance 4800 transcript derived fragments TDFs cDNA AFLP Dinari et al. (2013)


(Meuwissen et al. 2001). Therefore, it can be postulated thatgrowing approaches such as MARS, GS and genome wise asso-ciation (GWA) studies (Syvanen 2005, Myles et al. 2009, Rafal-ski 2010) would be more relevant than the family-based geneticlinkage mapping because the former methods require phenotyp-ing only once while testing variable alleles for their associationwith tolerance to abiotic stresses thereby minimizing the timeand painstaking work that is otherwise consumed in identifyingand further pinpointing the gene/QTLs responsible for thesestresses. It is important to emphasize that genomics-basedapproaches have led to the identification of QTLs and theircloning for subsequent use in breeding programmes (Salvi andTuberosa 2007). The various MB approaches deployed in differ-ent crops to tackle abiotic stresses and their subsequent impactsare discussed elaborately in various articles (Tuberosa and Salvi2006, Vij and Tyagi 2007, Cattivelli et al. 2008, Ashraf 2010,Varshney et al. 2011, Mir et al. 2012, Ashraf and Foolad 2013).In chickpea also, tremendous progress in genomics tools andtechnologies has leveraged the genomic resources particularlyfor abiotic stresses (Table 3).

Summary and OutlookThe global climate is changing drastically, and the unpredictablechanges in rainfall and an increase in temperature are causingsevere drought conditions. Further, high evapo-transpiration andscarcity of water have led to the depletion of the groundwater,hence creating problems of salinity. All considered, these factorshave put a strong barrier to the progress of development of stresstolerant cultivars. Notably, due to the severe pressure of globalclimate change and ever increasing demand for food production,implementation of high-throughput and cost-effective techniquesis required, which would invariably support the traditional breed-ing schemes. Therefore, immediate attention needs to be placedtowards (i) large scale exploration and characterization of theavailable germplasm for abiotic stresses tolerance, (ii) easyaccess to the high-throughput and robust screening techniques,(iii) standardization of selection criteria for various adaptive/physiological traits, (iv) utilization of genome-wide DNA markersystems and sequencing techniques to discover the beneficialalleles, (v) multilocation and multiyear testing under both con-trolled and stressed conditions and (vi) finally, pyramiding ofseveral component traits conditioning resistance against variousabiotic constraints. In summary, the growing ‘omics’ approaches,availability of community-oriented genetic and genomicresources for chickpea will enable the breeders to better correlatethe huge genotypic data with the extensive phenotypic informa-tion to derive the valid conclusions. Therefore, it is expected thatthe MB methods coupled with the recently available phenotypingplatforms will allow chickpea breeder to genetically manipulatethe abiotic stress and exploit the full potential of the crop tocombat against the food security and malnutrition-related chal-lenges and arranging the protein-rich quality food for over sevenbillion people across the globe.

Financial DisclosureNo financial assistance was received for this work.

Conflict of InterestsAll authors declare no conflict of interest.

Author ContributionUCJ conceived the idea and wrote the manuscript, SKC pro-vided input on breeding point of view, AB developed the Fig. 1and edited the manuscript, PSB provided input on physiologicalaspects, MSK provided input on genomics point of view, andDB provided input for overall improvement of the entire article.

ReferencesAhmad, F., P. Gaur, and J. Croser, 2005: Chickpea (Cicer ariatinum L.).In: R. Singh, and P. Jauhar (eds), Genetic Resources, ChromosomeEngineering and Crop Improvement- Grains Legumes, 185—214.CRC Press, USA.

Akhar, F. K., A. Bagheri, N. Moshtaghi, and A. Nezami, 2011: Theeffect of gamma radiation on freezing tolerance of chickpea (Ciceraretinum L.) at in vitro culture. J. Biol. Environ. Sci. 5, 63—70.

Ali, M., C. R. Jensen, V. O. Mogensen, M. N. Andersen, and I. E. Hen-son, 1999: Root signaling and osmotic adjustment during intermittentsoil drying sustain grain yield of field grown wheat. Field Crops Res.62, 35—52.

Ali, M. Y., L. Krishnamurthy, N. P. Saxena, O. P. Rupela, J. Kumar,and C. Johansen, 2002: Scope for genetic manipulation of mineralacquisition in chickpea. Plant Soil 245, 123—134.

Al-Mutawa, M. M., 2003: Effect of salinity on germination and seedlinggrowth of chickpea (Cicer arietinum L.) genotypes. Int. J. Agric. Biol.5, 226—229.

Ashraf, M., 2010: Inducing drought tolerance in plants: recent advances.Biotechnol. Adv. 28, 169—183.

Ashraf, M., and M. R. Foolad, 2013: Crop breeding for salt tolerance inthe era of molecular markers and marker-assisted selection. PlantBreeding 132, 10—20.

Bacon, M. A., 2004: Water Use Efficiency in Plant Biology. Blackwell,Oxford, UK.

Baker, N. R., 1991: Possible role of photosystem II in environmentalperturbations of photosynthesis. Physiol. Plant. 81, 563—570.

Baker, J. T., L. H. Allen Jr, K. J. Boote, and J. W. Jones, 1989:Response of soybean to air temperature and carbon dioxide concentra-tion. Crop Sci. 29, 98—105.

Bakht, J., A. Bano, and P. Dominy, 2006: The role of abscisic acid andlow temperature in chickpea (Cicer arietinum) cold tolerance. II.Effects on plasma membrane structure and function. J. Exp. Bot. 57,3707—3715.

Basu, P. S., and D. N. Singh, 2003: Physiology and abiotic stress inchickpea. In: M. Ali, S. Kumar, and N. B. Singh (eds), ChickpeaResearch in India, 137—167. Indian Institute of Pulses Research,Kanpur, India.

Basu, P. S., J. D. Berger, N. C. Turner, S. K. Chaturvedi, M. Ali, and K.H. M. Siddique, 2007: Osmotic adjustment of chickpea (Cicer arieti-num) is not associated with changes in carbohydrate composition orleaf gas exchange under drought. Ann. Appl. Biol. 150, 217—225.

Basu, P. S., M. Ali, and S. K. Chaturvedi, 2009: Terminal heat stressadversely affects chickpea productivity in Northern India- Strategies toimprove thermo tolerance in the crop under climate change. ISPRSArchives XXXVIII-8/W3 Workshop Proceedings: Impact of ClimateChange on Agriculture, 189—193. 23-25 February, New Delhi, India.

Bejiga, G., and Y. Anbessa, 1995: Water logging tolerance in chickpea.Int. Chickpea Pigeonpea Newslett. 2, 23—24.

Bell, M. J. N., 1993: Low night temperature response in peanut (Arachishypogaea L.). PhD Thesis. University of Guelph, pp. 170.

Benlloch-Gonzalez, M., J. Fournier, J. Ramos, and M. Benlloch, 2005:Strategies underlying salt tolerance in Halophytes are present inCynara carduncullus. Plant Sci. 168, 653—659.

Berger, J. D., 2007: Ecogeographic and evolutionary approaches toimproving adaptation of autumn-sown chickpea (Cicer arietinum L.)to terminal drought: the search for reproductive chilling tolerance.Field Crops Res. 104, 112—122.


Berger, J. D., and N. C. Turner, 2007: The ecology of chickpea. In: S.S. Yadav, R. J. Redden, W. Chen, and B. Sharma (eds), ChickpeaBreeding and Management, 47—71. CAB International, Wallingford,UK.

Berger, J. D., S. P. Milroy, N. C. Turner, K. H. M. Siddique, M. Imtiaz,and R. Malhotra, 2011: Chickpea evolution has selected for contrastingphenological mechanisms among different habitats. Euphytica 180,1—15.

Bernardo, R., 2008: Molecular markers and selections for complex traitsin plants: learning from the last 20 years. Crop Sci. 48, 1649—1664.

Bernardo, R., 2010: Genome wide selection with minimal crossing in selfpollinated crops. Crop Sci. 50, 624—627.

Bernardo, R., and A. Charcosset, 2006: Usefulness of gene informationin marker assisted recurrent selection: a simulation appraisal. Crop Sci.46, 614—621.

Black, C. C., R. H. Brown, and R. C. Moore, 1978: Plant photosynthe-sis. In: J. Dobereiner, R. M. Burns, and A. Hollander (eds), Limita-tions and Potentials for Biological Nitrogen Fixation in the Tropics, 95—110. Plenum Press, New York.

Blum, A., 1988: Plant Breeding for Stress Environments. CRC Press,Boca Raton, FL.

Blum, A., 1989: Osmotic adjustment and growth of barley genotypesunder drought stress. Crop Sci. 29, 230—233.

Blum, A., 2005: Drought resistance, water-use efficiency, and yieldpotential—are they compatible, dissonant, or mutually exclusive? Aust.J. Agric. Res. 56, 1159—1168.

Blum, A., J. X. Zhang, and H. T. Nguyen, 1999: Consistent differencesamong wheat cultivars in osmotic adjustment and their relationship toplant production. Field Crops Res. 64, 287—291.

Boyer, J. S., 1982: Plant productivity and environment. Science 218,443—448.

Brown, S. C., P. J. Gregory, P. J. M. Cooper, and J. D. H Keatinje,1989: Root and shoot growth and water use of chickpea (Cicer arieti-num) grown in dryland conditions: effects of sowing date and geno-type. J. Agric. Sci. 113, 41—49.

Bruggeman, A., A. Hamdy, F. Karajeh, T. Owei, and H. Touchan, 2003:Screening of some chi ckpea genotypes for salinity tolerance in aMedi terranean environment. In: A. Hamdy (ed.), Regional ActionProgramme (RAP): Water Resources Management and WaterSaving in Irrigated Agriculture (WASIAPROJECT), 171—179. CI-HEAM, Bari (Option s M�editerran�een nes: S�erie B. Etu deset Recher-ches; n. 44).

Canci, H., and C. Toker, 2009: Evaluation of yield criteria for droughtand heat resistance in chickpea (Cicer arietinum L.). J. Agron. CropSci. 19, 47—54.

Cattivelli, L., F. Rizza, F. W. Badeck, E. Mizzucotelli, A. M. Mastrange-lo, E. Francia, C. Mare, A. Tondelli, and A. M. Stanca, 2008: Droughttolerance improvement in crop plants: an integrated view to breedingto genomics. Field Crops Res. 105, 1—14.

Chamarthi, S. K., A. Kumar, T. D. Vuong, P. M. Gaur, M. W. Blair, H.T. Nguyen, and R. K. Varshney, 2011. Trait mapping and molecularbreeding. In: P. Aditya, and K. Jitender (eds), Biology and Breedingof Food Legumes, 296—313. CABI, Wellingford, UK.

Chandra, S., H. K. Buhariwalla, J. Kashiwagi, S. Harikrishna, K. R.Sridevi, L. Krishnamurthy, R. Serraj, and J. H. Crouch, 2004: Iden-tifying QTL-linked markers in marker-deficient crops. In: 4thInterna-tional Crop Science Congress, 26 Sep–1 Oct 2004, Brisbane,Australia.

Chaves, M. M., 1991: Effects of water deficits on carbon assimilation. J.Exp. Bot. 42, 1—16.

Chaves, M. M., J. S. Pereira, and J. Maroco, 2003: Understanding plantresponse to drought–from genes to the whole plant. Funct. Plant Biol.30, 239—264.

Chaves, M. M., J. Flexas, and C. Pinheiro, 2009: Photosynthesis underdrought and salt stress: regulation mechanisms from whole plant tocell. Ann. Bot. 103, 551—560.

Chohan, A., and S. K. Raina, 2011: Comparative studies on morphologi-cal and biochemical characters of chickpea genotypes under chillingstress. J. Environ. Biol. 39, 189—194.

Ciardi, J. A., J. Deikman, and M. D. Orzolek, 1997: Increased ethylenesynthesis enhances chilling tolerance in tomato. Physiol. Plant. 101,333—340.

Clarke, H., and K. H. M. Siddique, 2003: Chilling tolerance in chickpea– Novel methods for crop improvement. In: R. N. Sharma, M. Yasin,S. L. Swami, M. A. Khan, and A. J. William (eds), InternationalChickpea Conference, 5—12. Indira Gandhi Agricultural University,Raipur, India.

Clarke, H. J., T. N. Khan, and K. H. M. Siddique, 2004: Pollen selectionfor chilling tolerance at hybridisation leads to improved chickpea culti-vars. Euphytica 139, 65—74.

Cowie, A., R. S. Jessop, and D. A. MacLeod, 1995: A study of waterlogging damage in Australian chickpea cultivars Int. Chickpea Pigeon-pea Newslett. 2, 22—23.

Cowie, A. L., R. S. Jessop, and D. A. Macleod, 1996: Effect of water-logging on chickpeas. Plant Soil 183, 97—103.

Croser, J. S., H. J. Clarke, K. H. M. Siddique, and T. N. Khan, 2003:Low temperature stress: implications for chickpea (Cicer arietinum L.)improvement. Crit. Rev. Plant Sci. 22, 185—219.

Deokar, A. A., V. Kondawar, P. K. Jain, M. S. Karuppyil, N. L. Raju,V. Vadez, R. K. Varshney, and R. Srinivasan, 2011: Comparativeanalysis of expressed sequence tags (ESTs) between drought-tolerantand –susceptible genotypes of chickpea under terminal drought stress.BMC Plant Biol. 11, 70.

Devasirvatham, V., D. K. Y. Tan, R. M. Trethowan, P. M. Gaur, and N.Mallikarjuna, 2010: Impact of high temperature on the reproductivestage of chickpea. In ‘Food Security from Sustainable Agriculture’.Proceedings of the 15th Australian Society of Agronomy Conference,15-18 November 2010, Lincoln, New Zealand.

Devasirvatham, V., P. Gaur, N. Mallikarjuna, T. N. Raju, R. M. Tretho-wan, and D. K. Y Tan, 2012: Effect of high temperature on the repro-ductive development of chickpea genotypes under controlledenvironments. Funct. Plant Biol. 39, 1009—1018.

Devasirvatham, V., P. Gaur, N. Mallikarjuna, T. N. Raju, R. M. Tretho-wan, and D. K. Y. Tan, 2013: Reproductive biology of chickpearesponse to heat stress in the field is associated with the performancein controlled environments. Field Crops Res. 142, 9—19.

Dias, A. S., and F. C. Lidon, 2009: Evaluation of grain filling rate andduration in bread and durum wheat, under heat stress after anthesis. J.Agron. Crop Sci. 195, 137—147.

Dinari, A., A. Niazi, A. R. Afsharifar, and A. Ramezani, 2013: Identifi-cation of upregulated genes under cold stress in cold-tolerant chickpeausing the cDNAAFLP approach. PLoS ONE 8, e52757.

Dua, R., 1992: Differential response of chickpea (Cicer arietinum) geno-types to salinity. J. Agric. Sci. 119, 367—371.

Dua, R. P., 2001: Genotypic variations for low and high temperaturetolerance in gram (Cicer arietinum). Indian J. Agric. Sci. 71, 561—566.

Dua, R. P., and P. C. Sharma, 1995: Salinity tolerance of kabuli and desichickpea genotypes. Int. Chickpea Pigeonpea Newslett. 2, 19—22.

Esfahani, M. N., and A. Mostajeran, 2011: Rhizobial strain involvementin symbiosis efficiency of chickpea–rhizobia under drought stress:plant growth, nitrogen fixation and antioxidant enzyme activities. ActaPhysiol. Plant. 33, 1075—1083.

Ethington, S. R., T. M. Crosbie, M. D. Edwards, R. S. Reiter, and J. K.Bull, 2007: Molecular markers in commercial breeding program. CropSci. 47, S154—S163.

Evan, P. T., and R. L. Malmberg, 1989: Do polyamines have roles inplant development? Annu. Rev. Plant Physiol. Plant Mol. Biol. 40,235—269.

FAOSTAT, 2012: Available at: http://faostat3.fao.org/home/index.html(last accessed on November 16, 2013).

Farshadfar, E., S. H. Sabaghpour, and N. Khaksar, 2008: Inheritance ofdrought tolerance in chickpea (Cicer arietinum L.) using joint scalingtest. J. Appl. Sci. 8, 3931—3937.

Fisher, K. S., E. C. Johanson, and G. O. Edmeades, 1982: Breeding andselection for drought resistance in tropical maize. In: Dought Resis-tance in Crops with Emphasis on Rice, 377—399. IRRI, Manila, Phil-ippines.


Flores, H. E., 1991: Changes in polyamines metabolism in response toabiotic stress. In: R. D. Slocum, and H. E. Flores (eds), Biochemistryand Physiology of Polyamines in Plants, 214—228. CRC Press, BocaRaton.

Flowers, T. J., P. M. Gaur, C. L. L. Gowda, L. Krishnamurth, S. Sriniva-san, K. H. M. Siddique, N. C. Turner, V. Vadez, R. K. Varshney, andT. D. Colmer, 2010: Salt sensitivity in chickpea. Plant, Cell Environ.33, 490—509.

Fokar, M., A. Blum, and H. T. Nguyen, 1998: Heat tolerance in springwheat. II. Grain filling. Euphytica 104, 9—15.

Fridovich, I., 1986: Super oxide dismutases. In: A. Merister (ed.),Advances in Enzymology and Related Areas of Molecular Biology,61—97. John Wiley & Sons, New York.

Frisch, M., M. Bohn, and A. E. Melchinger, 1999: Minimal sample sizeand optimal positioning of flanking markers in marker assisted back-crossing for transfer of target gene. Crop Sci. 39, 967—975.

Ganjeali, A., H. Porsa, and A. Bagheri, 2011: Assessment of Iranianchickpea (Cicer arietinum L.) germplasm for drought tolerance. Agr.Water Manage. 98, 1477—1484.

Garthwaite, A. J., R. von Bothmer, and T. D. Colmer, 2005: Salt toler-ance in wild Hordeum species is associated with restricted entry ofNa+ and Cl� into the shoot. J. Exp. Bot. 56, 2365—2378.

Gaur, P. M., L. Krishnamurty, and J. Kashiwagi, 2008: Improvementdrought-avoidance root traits in chickpea (Cicer arietinum L.)-currentstatus of research at ICRISAT. Plant Prod. Sci. 1, 3—11.

Gaur, P. M., S. K. Chaturvedi, S. Tripathi, C. L. L. Gowda, L. Krishna-murthy, V. Vadez, N. Mallikarjuna, and R. K. Varshney, 2010:Improving heat tolerance in chickpea to increase its resilience to cli-mate change. 5th International Food Legumes Research Conference &7th European Conference on Grain Legume. April 26-30, 2010. Antal-ya, Turkey.

Gaur, P. M., A. K. Jukanti, and R. K. Varshney, 2012: Impact of genomictechnologies on chickpea breeding strategies. Agronomy 2, 199—221.

Gigon, A., A. R. Matos, D. Laffray, Z. F. Yasmine, and A. T. PhamThi, 2004: Effect of drought stress on lipid metabolism in the leavesof arabidopsis thaliana (Ecotype Columbia). Ann. Bot. 94, 345—351.

Gil, J., M. T. Moreno, S. Nadal, D. Luna, and A. De Haro, 1996: Vari-ability of some physico-chemical characters in desi and kabuli chick-pea types. J. Sci. Food Agric. 71, 179—184.

Graham, D., and B. D. Patterson, 1982: Response of plant to low, non-freezing temperatures: protein, metabolism and acclimation. Annu.Rev. Plant Physiol. 33, 347—372.

Gupta, P. K., J. Kumar, R. R. Mir, and A. Kumar, 2010: Marker assistedselection as a component of conventional plant breeding. Plant BreedRev. 33, 145—217.

Hallgren, J. E., and G. Oquest, 1990: Adaptation to low temperatures.In: R. G. Alscher, and J. R. Cumming (eds), Stress Responses inPlants: Adaptation and Acclimation Mechanisms, 265—293. Wiley-Liss Inc., New York.

Halliwell, B., and J. M. C. Gutteridge, 1989: Free Radicals in Biologyand Medicine, 2nd edn. Clarendon Press. Oxford, UK.

Harb, A., A. Krishnan, M. M. R. Ambavaram, and A. Pereira, 2010:Molecular and physiological analysis of drought stress in arabidopsisreveals early responses leading to acclimation in plant growth. PlantPhysiol. 154, 1254—1271.

Hassanein, A. A., 2000: Physiological responses induced by shock andgradual salinization in rice (Oryza sativa L.) seedlings and the possibleroles played by glutathione treatment. Acta Bot. Hung. 42, 139—159.

Hayashi, H., and N. Murata, 1998: Genetically engineered enhancementof salt tolerance in higher plants. In: N. Sato Murata (ed.), StressResponse of Photosynthetic Organism: Molecular Mechanism andMolecular Regulation, 133—148. Elsevier, Amsterdam.

Hodgson, R. A., and J. K. Raison, 1991: Superoxide production by thy-lakoid during chilling and its implication in the susceptibility of plantsto chilling induced photo inhibition. Planta 183, 222—228.

Hospital, F., 2003. Marker assisted breeding. In: H. J. Newbury (ed.),Plant Molecular Breeding, 30—56. Blackwell Publishing, Carlton.

Hospital, F., and A. Charcosset, 1997: A marker assisted introgression ofquantitative trait loci. Genetics147, 1469—1485.

Ibrikci, H., S. Knewtson, and M. A. Grusak, 2003: Chickpea leaves asvegetable green for human: evaluation of mineral composition. J. Sci.Food Agric. 83, 945—950.

Iliadis, C., 1990: Chickpea production in Greece. Options M�editer-ran�eennes S�erie S�eminaires 9, 141—143.

Jaganathan, D., M. Thudi, S. Azam, P. Gaur, H. Nguyen, T. Sutton, andR. K. Varshney, 2013: Towards fine mapping of drought tolerancerelated QTL region in chickpea using genotyping by sequencing(GBS) approach. PAG XXI Conference Abstract PO362 January 2013.Available at: http://pag.confex.com/pag/xxi/webprogram/Paper7538.html (last accessed on January 16, 2013).

Jain, D., and D. Chattopadhyay, 2010: Analysis of gene expression inresponse to water deficit of chickpea (Cicer arietinum L.) varieties dif-fering in drought tolerance. BMC Plant Biol. 10, 24.

Jain, M., G. Misra, R. K. Patel, P. Priya, S. Jhanwar, A. W. Khan, N.Shah, V. K. Singh, R. Garg, G. Jeena, M. Yadav, C. Kant, P. Sharma,G. Yadav, S. Bhatia, A. K. Tyagi, and D. Chattopadhyay, 2013: Adraft genome sequence of the pulse crop chickpea (Cicer arietinumL.). Plant J. 74, 715—729.

Jayashree, B., H. K. Buhariwalla, S. Shinde, and H. C. Jonathan, 2005:A legume genomics resource: the chickpea root expressed sequencetag database. Electron. J. Biotechnol. 8, 128—133.

Kanouni, H., H. A. Kazemi, M. Moghadam, and M. R. Neyshabouri,2002: Selection of Chickpea (Cicer arietinum L.) entries for droughtresistance. J. Agric. Sci. 12, 109—121.

Kanouni, H., M. Khalily, and R. S. Malhotra, 2009: Assessment of coldtolerance of chickpea at rainfed highlands of Iran American-Eurasian.J. Agric. Environ. Sci. 5, 250—254.

Kashiwagi, J., L. Krishnamurthy, H. D. Upadhyaya, H. Krishna, S.Chandra, V. Vadez, and R. Serraj, 2005: Genetic variability ofdrought-avoidance root traits in the mini-core germplasm collection ofchickpea (Cicer arietinum L.). Euphytica 146, 213—222.

Kashiwagi, J., L. Krishnamurthy, J. H. Crouch, and R. Serraj, 2006a:Variability of root length density and its contributions to seed yield inchickpea (Cicer arietinum L) under terminal drought stress. FieldCrops Res. 95, 171—181.

Kashiwagi, J., L. Krishnamurthy, S. Singh, P. M. Gaur, H. D. Up-adhyaya, J. D. S. Panwar, P. S. Basu, O. Ito, and S. Tobita, 2006b:Relationship between transpiration efficiency and carbon isotopediscrimination in chickpea (Cicer arietinum L.). J. SAT Agric. Res. 2,1—3.

Kashiwagi, J., L. Krishnamurty, P. M. Gaur, S. Chandra, and H. D. Up-adhyaya, 2008: Estimation of gene effects of the drought avoidanceroot characteristics in chickpea (C. arietinum L.). Field Crops Res.105, 64—69.

Kashiwagi, J., L. Krishnamurthy, P. M. Gaur, H. D. Upadhyaya, R. K.Varshney, and S. Tobita, 2013: Traits of relevance to improve yieldunder terminal drought stress in chickpea (C. arietinum L.). FieldCrops Res. 145, 80—95.

Katerji, N., J. W. van Hoorn, A. Hamdy, M. Mastrorilli, T. Oweis,and R. S. Malhotra, 2001: Response to soil salinity of two chickpeavarieties differing in drought tolerance. Agr. Water Manag. 50,83—96.

Katerji, N., J. W. van Hoorn, A. Hamdy, and M. Mastrorilli, 2003: Salin-ity effect on crop development and yield, analysis of salt toleranceaccording to several classification methods. Agr. Water Manag. 62,37—66.

Katerji, N., J. W. van Hoorn, A. Hamdy, M. Mastrorilli, and T. Oweis,2005: Salt tolerance analysis of chickpea, faba bean and durum wheatvarieties – I. Chickpea and faba bean. Agric. Water Manag. 72,177—194.

Kaur, S., A. K. Gupta, N. Kaur, J. S. Sandhu, and S. K. Gupta, 2009:Antioxidative enzymes and sucrose synthase contribute to cold stresstolerance in chickpea. J. Agronomy Crop Sci. 195, 393—397.

Krishnamurthy, L., C. Johansen, and O. Ito, 1996: Genotypic variation inroot system development and its implications for drought resistance inchickpea. In: O. Ito, C. Johansen, J. J. Adu-Gyamfi, K. Katayama, J.V. D. K. Kumar Rao, and T. J. Rego (eds), 9 in Dynamics of Rootand Nitrogen in Cropping System of the Semi-arid Tropics, 235—250.


Japan International research Centre for Agricultural Sciences, Tsukuba,Japan.

Krishnamurthy, L., J. Kashiwagi, H. D. Upadhyaya, and R. Serraj, 2003:Genetic diversity of drought avoidance root traits in the mini-coregermplasm collection of chickpea. Int. Chickpea Pigeonpea Newslett.10, 21—24.

Krishnamurthy, L., V. Vadez, M. Jyotsna Devi, R. Serraj, S. N. Nigam,M. S. Sheshshayee, S. Chandra, and R. Aruna, 2007: Variation in tran-spiration efficiency and its related traits in a groundnut (Arachis hypo-gaea L) mapping population. Field Crops Res. 13, 189—197.

Krishnamurthy, L., P. M. Gaur, P. S. Basu, S. K. Chaturvedi, S. Tripathi,V. Vadez, R. K. Varshney, and C. L. L. Gowda, 2011: Large geneticvariation for heat tolerance in the reference collection of chickpea(Cicer arietinum L.) germplasm. Plant Genet. Res. 9, 59—69.

Krishnamurthy, L., J. Kashiwagi, H. D. Upadhyaya, C. L. L. Gowda, P.M. Gaur, S. Singh, R. Purushothaman, and R. K. Varshney, 2013a:Partitioning coefficient–a trait that contributes to drought tolerance inchickpea. Field Crops Res. 149, 354—365.

Krishnamurthy, L., J. Kashiwagi, S. Tobita, O. Ito, H. D. Upadhyaya, C.L. L. Gowda, P. M. Gaur, M. S. Sheshshayee, S. Singh, V. Vadez,and R. K. Varshney, 2013b: Variation in carbon isotope discriminationand its relationship with harvest index in the reference collection ofchickpea germplasm. Funct. Plant Biol. 40, 1350—1361.

Krishnamurty, L., J. Kashiwagi, P. M. Gaur, H. D. Upadhyaya, and V.Vadez, 2010: Sources of tolerance to terminal drought in the chickpea(Cicer arietinum L.) minicore germplasm. Field Crops Res. 119,322—330.

Kumar, J., and S. Abbo, 2001: Genetics of flowering time in chickpeaand its bearing on productivity in semi arid environments. Adv.Agron. 72, 107—138.

Kumar, J., and B. V. Rao, 1996: Super early chickpea developed atICRISAT Asia Center. Int. Chickpea Pigeonpea Newslett. 3, 17—18.

Kumar, J., and H. A. van Rheenen, 2000: A major gene for time offlowering in chickpea. J. Hered. 91, 67—68.

Kumar, S., G. Kaur, and H. Nayyar, 2007: Exogeneous application ofabscisic acid improves cold tolerance in chickpea (Cicer arietinum L.).J. Agron. Crop Sci. 194, 449—456.

Kumar, N., A. S. Nandwal, S. Devi, K. D. Sharma, A. Yadav, and R. S.Waldia, 2010a: Root characteristics, plant water status and CO2exchange in relation to drought tolerance in chickpea. J. SAT Agric.Res. 8, 1—5.

Kumar, S., H. Nayyar, R. K. Bhanwara, and H. D. Upadhyaya, 2010b:Chilling stress effects on reproductive biology of chickpea. J. SATAgric. Res. 8, 1—14.

Kumar, S., N. Kaushal, H. Nayyar, and P. M. Gaur, 2012: Abscisic acidinduces heat tolerance in chickpea (Cicerarietinum L.) seedlings byfacilitated accumulation of osmoprotectants. Acta Physiol. Plant. 34,1651—1658.

Kurets, V. K., and E. G. Popov, 1988: Evaluating the requirements of agenotype in respect of environmental conditions. In: Diagnostika urtoi-chivosti rastenii stressovym vozdeistviyam, Leningrad, USSR, 222—227.

Labidi, N., H. Mahmoudi, M. Dorsaf, I. Slama, and C. Abdelly,2009: Assessment of intervarietal differences in drought tolerance inchickpea using both nodule and plant traits as indicators. JPBCS 1,80—86.

Lauter, D. J., and D. N. Munns, 1986: Salt resistance of chickpeagenotypes in solutions salinized with NaCl or Na2SO4. Plant Soil 95,271—279.

Lecoeur, J., J. Wery, and O. Turc, 1992: Osmotic adjustment as a mech-anism of dehydration postponement in chickpea (Cicer arietinum L.)leaves. Plant Soil 144, 177—189.

Levitt, J., 1969: Growth and survival of plants at extreme of tempera-ture–a unified concept. Symp. Soc. Exp. Biol. 23, 395—448.

Levitt, J., 1972: Responses of Plants to Environmental Stresses. Aca-demic Press, New York.

Loomis, R. S., and D. J. Connor, 1992: Crop Ecology: Productivity andManagementin Agricultural Systems, 224—256. Cambridge UniversityPress, Cambridge, UK.

Mafakheri, A., A. Siosemardeh, B. Bahramnejad, P. C. Struik, and Y.Sohrabi, 2011: Effect of drought stress and subsequent recovery onprotein, carbohydrate contents, catalase and peroxidase activities inthree chickpea (Cicer arietinum) cultivars. Aust. J. Crop Sci. 5,1255—1260.

Mafekheri, A., A. Siosemardeh, B. Bahramnejad, P. C. Struik, and Y.Sohrabi, 2010: Effect of drought stress on yield, proline and chloro-phyll contents in three chickpea cultivars. Aust. J. Crop Sci. 4,580—585.

Magyar, G., A. Kun, B. Oborny, and J. F. Stuefer, 2007: Importance ofplasticity and decision-making strategies for plant resource acquisitionin spatio-temporally variable environments. New Phytol. 174,182—193.

Malhotra, R. S., and K. B. Singh, 1991: Gene action for cold tolerancein chickpea. Theor. Appl. Genet. 5, 598—601.

Maliro, M. F. A., D. McNeil, J. Kollmorgen, C. Pittock, and B. Redden,2004: Screening chickpea (Cicer arietinumL.) and wild relatives germ-plasm from diverse sources for salt tolerance. New directions for adiverse planet. In: Proceedings of the 4th International Crop ScienceCongress, Brisbane, Australia (September 26–October 1). Available at:http://www.cropscience.org.au.

Maliro, M. F. A., D. MacNeil, B. Redden, J. F. Kollmorgen, and C. Pit-tock, 2008: Sampling strategies and screening of chickpea (Cicer ariet-inum L.) germplasm for salt tolerance. Genet. Resour. Crop Evol. 55,53—63.

Mannur, D. M., P. M. Salimath, and M. N. Mishra, 2009: Evaluation ofsegregating populations for drought related morphological and physio-logical traits in chickpea. J. Food Legume 22, 233—238.

Mantri, N. L., R. Ford, T. E. Coram, and E. C. Pang, 2007: Transcrip-tional profiling of chickpea genes differentially regulated in responseto high-salinity, cold and drought. BMC Genomics 8, 303.

McDonald, G. K., and G. M. Paulsen, 1997: High temperature effects onphotosynthesis and water relations of grain legumes. Plant Soil 196,47—58.

McKersie, B. D., and S. R. Bowley, 1997. Active oxygen and freezingtolerance in transgenic plants. In: P. H. Li, and T. H. H. Chen (eds).Plant Cold Hardiness, Molecular Biology, Biochemistry and Physiol-ogy. Plenum, New York, pp. 203—214.

Meuwissen, T., B. J. Hayes, and M. E. Goddard, 2001: Prediction oftotal genetic value using genome wide-dense marker maps. Genetics157, 1819—1829.

Millan, T., H. J. Clarke, K. H. M. Siddique, H. K. Bhuriwalla, P. M.Gaur, J. Kumar, J. Gil, G. Kahl, and P. Winter, 2006: Chickpeamolecular breeding: new tools and concepts. Euphytica 147, 81—103.

Mir, R. R., M. Zaman-Allah, N. Sreenivasulu, R. Trethowan, and R. K.Varshney, 2012: Integrated genomics, physiology and breedingapproaches for improving drought tolerance in crop. Theor. Appl.Genet. 125, 625—645.

Moinuddin, and R. Khanna-Chopra, 2004: Osmotic adjustment in chickpeain relation to seed yield and yield parameters. Crop Sci. 44, 449—455.

Molina, C., B. Rotter, R. Horres, S. M. Udupa, B. Besser, L. Bellarmino,M. Baum, H. Matsumura, R. Terauchi, G. Kahl, and P. Winter, 2008:SuperSAGE: the drought stress- responsive transcriptome of chickpearoots. BMC Genomics 9, 553.

Molina, C., M. Zaman-Allah, F. Khan, N. Fatnassi, R. Horres, B. Rotter,D. Steinhauer, L. Amenc, J. J. Drevon, P. Winter, and G. Kahl, 2011:The salt-responsive transcriptome of chickpea roots and nodules viadeep Super SAGE. BMC Plant Biol. 11, 31.

Monteiro de Paula, F., A. T. Pham Thi, J. Vieira da Silva, A. M. Justin,C. Demandre, and P. Mazliak, 1990: Effects of water stress on themolecular species composition of polar lipids from Vigna unguiculataL. leaves. Plant Sci. 66, 185—193.

Morgan, J. M., 1984: Osmoregulation and water stress in higher plants.Annu. Rev. Plant Physiol. 35, 299—319.

Morgan, J. M., 2000: Increases in grain yield of wheat by breeding foran osmoregulation gene: relationship to water supply and evaporativedemand. Aust. J. Agric. Res. 51, 971—978.

Morgan, J. M., and A. G. Condon, 1986: Water use, grain yield andosmoregulation in wheat. Aust. J. Plant Physiol. 13, 523—532.


Morgan, P. W., and M. C. Drew, 1997: Ethylene and plant response tostress. Physoil. Plant 100, 620—630.

Morgan, J. M., B. Rodriguezmaribona, and E. J. Knights, 1991: Adapta-tion to water-deficit in chickpea breeding lines by osmoregulation –relationship to grain yields in the field. Field Crops Res. 27, 61—70.

Munnes, R., and R. A. James, 2003: Screening methods for salinity toler-ance: a case study with tetraploid wheat. Plant Soil 253, 201—218.

Munns, R., 2002: Comparative physiology of salt and water stress. Plant,Cell Environ. 20, 239—250.

Munns, R., 2005: Genes and salt tolerance: bringing them together. NewPhytol. 167, 645—663.

Murata, N., 1983: Molecular species composition of phosphatidylglyce-rols from chilling sensitive and chilling resistant plants. Plant CellPhysiol. 24, 81—86.

Myles, S., J. Peiffer, P. J. Brown, E. S. Ersoz, Z. Zhang, D. E. Costich, andE. S. Buckler, 2009: Association mapping: critical considerations shiftfrom genotyping to experimental design. Plant Cell 21, 2194—2202.

Nakano, H., T. Momonoki, T. Miyashige, H. Otsuka, T. Hanada,A. Sugimoto, H. Nakagawa, M. Matsuoka, T. Terauchi, M. Kobayashi,M. Oshiro, K. Yasuda, N. Vanichwattanarumruk, S. Chotechuen, andD. Boonmalison, 1997: ‘Haibushi’, a new variety of snap bean tolerantto heat stress. JIRCAS J. Sci. Pap. 5, 1—12.

Nakano, H., M. Kobayashi, and T. Terauchi, 1998: Sensitive stages toheat stress in pod setting of common bean (Phaseolus vulgaris L.).Jpn J. Tropic. Agric. 42, 72—84.

Nayyar, H., K. Chander, S. Kumar, and T. Bains, 2005: Glycine betainemitigates cold stress damage in Chickpea. Agron. Sustain. Dev. 25,381—388.

Nayyar, H., T. Bains, and S. Kumar, 2005: Low temperature induced flo-ral abortion in chickpea: relationship to abscisic acid and cryoprotec-tants in reproductive organs. Environ. Exp. Bot. 53, 39—47.

Nezami, A., A. Bagheri, H. Rahimian, M. Kafi, and M. N. Mahalat,2007: Evaluation of freezing tolerance of chickpea (Cicer arietinumL.) genotypes under controlled conditions. J. Sci. Technol. Agric. Nat.Res. 10, 257—269.

Nicotra, A. B., O. K. Atkin, S. P. Bonser, A. M. Davidson, E. J. Finne-gan, U. Matesius, P. Poot, M. D. Purugganan, C. L. Richards, F. Val-ladares, and M. van Kleunen, 2010: Plant phenotypic plasticity in achanging climate. Trends Plant Sci. 15, 684—692.

Omran, R. G., 1980: Peroxidase levels and the activities of catalase, per-oxidase and indolacetic acid oxidase during and after chilling cucum-ber seedling. Plant Physiol. 65, 407—408.

Palta, J. A., A. Ganjeali, N. C. Turner, and K. H. M. Siddique, 2010:Effects of transient subsurface water logging on root growth, plant bio-mass and yield of chickpea. Agr. Water Manag. 97, 1469—1476.

Parida, S. K., and A. B. Das, 2005: Salt tolerance and salinity effects onplants. Ecotoxicol. Environ. Saf. 60, 324—349.

Parmeshwarappa, S. G., P. M. Salimath, H. D. Upadhyaya, S. S. Patil, S.T. Kajjidoni, and B. C. Patil, 2010: Characterization of drought toler-ant accessions identified from the minicore of chickpea (Cicer arieti-num L.). Indian J. Genet. 70, 125—131.

Pham-Thi, A. T., C. Borrel-Flood, J. Vieira da Silva, A. M. Justin, andP. Mazliak, 1987: Effects of drought on [1-14C]-oleic and [1-14C]-li-noleic acid desaturation in cotton leaves. Physiol. Plant. 69, 147—150.

Pinheiro, C., and M. M. Chaves, 2011: Photosynthesis and drought: canwe make metabolic connections from available data? J. Exp. Bot. 62,869—882.

Pouresmael, M., R. A. Khavari-Nejad, J. Mozafari, F. Najafi, and F. Mo-radi, 2013: Efficiency of screening criteria for drought tolerance inchickpea. Arch. Agronomy Soil Sci., 59, 1675—1693.

Prasad, T. K., M. D. Anderson, B. A. Martin, and C. R. Steward, 1994:Evidence for chilling induced oxidative stress maize seedling and aregulatory role for hydrogen peroxide. Plant Cell 6, 65—75.

Prasad, P. V. V., K. J. Boote, L. H. Jr Allen, and J. G. M. Thomas,2002: Effects of elevated temperature and carbon dioxide on seed-setand yield of kidney bean (Phaseolus vulgaris L.). Glob. Change Biol.8, 710—721.

Prasad, P. V. V., K. J. Boote, L. H. Allen Jr, and J. G. M. Thomas,2003: Super-optimal temperatures are detrimental to reproductive pro-

cesses and yield of peanut under both ambient and elevated carbondioxide. Glob. Change Biol. 9, 1775—1787.

Rafalski, J. A., 2010: Association genetics in crop improvement. Curr.Opin. Plant Biol. 13, 174—180.

Ramoliya, P., H. Patel, and A. N. Pandey, 2004: Effect of salinizationof soil on growth and macro and micro nutrient accumulation inseedling of Salvadora persica (salvadoraceae). For. Ecol. Manage.202, 181—193.

Rehman, A. U., R. S. Malhotra, K. Bett, B. Taran, R. Bueckert, and T.D. Warkentin, 2011: Mapping QTL associated with traits affectinggrain yield in chickpea (Cicer arietinum L.) under terminal droughtstress. Crop Sci. 51, 450—463.

Ribaut, J. M., and M. Ragot, 2007: Marker assisted selection to improvedrought adaptation in maize: the backcross approach, perspective, limi-tations and alternatives. J. Exp. Bot. 58, 351—360.

Ribaut, J. M., M. C. de Vicente, and X. Delannay, 2010: Molecularbreeding in developing countries: challenges and perspective. Curr.Opin. Plant Biol. 13, 1—6.

Rikin, A., and A. E. Richmond, 1976: Amelioration of chilling injuriesin cucumber seedlings by abscisic acid. Physiol. Plant. 38, 95—97.

Ryan, J., 1997: A global perspective on pigeonpea and chickpea sustain-able production system: present status and future potential. In: A. As-thana, and A. M. Kanpur (eds), Recent Advances in Pulses Researchin India, 1—31. Indian Society for Pulses Research and Development,Kalyanpur, Kanpur.

Sabaghpour, S. H., A. A. Mahmodi, A. Saeed, M. Kamel, and R. S.Malhotra, 2006: Study on chickpea drought tolerance lines under dry-land condition of Iran. Indian J. Crop Sci. 1, 70—73.

Saeed, A., R. Darvishzadeh, H. Hovsepyan, and A. Asatryan, 2010: Tol-erance to freezing stress in Cicer accessions under controlled and fieldconditions. African J. Biotech. 9, 2618—2626.

Salvi, S., and R. Tuberosa, 2007: Cloning QTLs in plants. In: R. K.Varshney, and R. Tuberosa (eds), Genomic Assisted Crop Improve-ment, 207—226. Springer, New York.

Samineni, S., K. H. M. Siddique, P. Gaur, and T. D. Colmer, 2011: Saltsensitivity of the vegetative and reproductive stages in chickpea (Cicerarietinum L.): podding is a particularly sensitive stage. Environ. Exp.Bot. 71, 260—268.

Sandhu, J. S., T. S. Bains, and P. S. Sidhu, 2002: Evaluation of superearly chickpea genotypes for vegetable purpose as a catch crop. Int.Chickpea Pigeonpea Newslett. 9, 10—12.

Sarwar, N., S. Yousaf, and F. F. Jamil, 2006: Induction of salt tolerance inchickpea by using simple and safe chemicals. Pak. J. Bot. 38, 325—329.

Sassenrath, G. E., G. E. Ort, and A. R. Portis, 1990: Impaired reductive acti-vation of stomatal biophosphatases in tomato leaves following low tem-perature exposure at high light. Arch. Biochem. Biophy. 282, 302—308.

Savithri, K. S., P. S. Ganapathy, and S. K. Sinha, 1980: Sensitivity tolow tolerance in pollen germination and fruit set in Cicer arietinum L.J. Exp. Bot. 31, 475—481.

Saxena, N. P., 1984: Chickpea. In: P. R. Goldsworthy, and N. M. Fisher(eds), The physiology of Tropical Field Crops, pp. 419—452. Wiley,Sussex, UK.

Saxena, N. P., 2003: Management of drought in chickpea- a holisticapproach. In: N. P. Saxena (ed.), Management of AgriculturalDrought-Agronomic and Genetic Options, 103—122. Oxford & IBHPublishing Co. Pvt. Ltd., New Delhi.

Saxena, M. C., and K. B. Singh, 1987: The Chickpea, 399 p. C.A.BInternational, Wallingford, UK.

Saxena, M. C., N. P. Saxena, and A. K. Mohammed, 1988: High temper-ate stress. In: R. J. Summerfield (ed.), World Crops: Cool-SeasonFood Legumes, 845—856. Kluwer Academic Publisher, Dordrecht, theNetherlands.

Saxena, N. P., L. Krishnamurthy, and C. Johansen, 1993: Registration ofa drought-resistant chickpea germplasm. Crop Sci. 33, 1424.

Saxena, N. P., L. Krishnamurthy, and C. Johansen, 1994: Registration ofa drought resistant chickpea germplasm. Crop Sci. 33, 1424.

Serraj, R., and T. R. Sinclair, 2002: Osmolyte accumulation: can it reallyhelp increase crop yield under drought condition. Plant, Cell Environ.25, 333—341.


Serraj, R., L. Krishnamurthy, J. Kashiwagi, J. Kumar, S. Chandra, and J.H. Crouch, 2004a: Variation in root traits of chickpea (Cicer arietinumL.) grown under terminal drought. Field Crops Res. 88, 115—127.

Serraj, R., L. Krishnamurthy, and H. D. Upadhyaya, 2004b: Screeningchickpea mini-core germplasm for tolerance to soil salinity. Int. Chick-pea Pigeonpea Newslett. 11, 29—32.

Sharkey, T. D., 2005: Effect of moderate heat stress on photosynthesis:importance of thylakoid reactions, rubisco deactivation, reactive oxy-gen species and thermo tolerance provided by isoprene. Plant, CellEnviron. 28, 269—277.

Sharma, S. K., H. R. Manchanda, and J. P. Singh, 1982: Note on theperformance of some chickpea varieties grown on chloride dominantsaline soils. Indian J. Agric. Sci. 52, 405—407.

Siddique, K. H. M., and R. H. Sedgley, 1986: Chickpea (Cicer arietinumL.), a potential grain legume for South-Western Australia: seasonalgrowth and yield. Aust. J. Agric. Res. 37, 245—261.

Siddique, K. H. M., S. P. Loss, and B. D. Thomson, 1997: Cool-seasongrain legumes in dry land Mediterranean environments of westernAustralia: significance of early flowering. In: N. P. Saxena, and C. Jo-hansen (eds), Management of Drought in Grain Legumes, 189—199.ICARDA, Aleppo, Syria.

Siddique, K. H. M., S. P. Loss, K. L. Regan, and R. Jettner, 1999:Adaptation of cool season grain legumes in Mediterranean-typeenvironments of south-western Australia. Aust. J. Agric. Res. 50,375—387.

Singh, K. B., 1993: Problems and prospects of stress resistance breedingin chickpea. In: K. B. Singh, and M. C. Saxena (eds), Breeding forStress Tolerance in Cool Season Food Legumes, 17—37. Wiley, Chi-chester.

Singh, A. K., 2004: The physiology of salt tolerance in four genotypesof chickpea during germination. J. Agric. Sci. Technol. 6, 87—93.

Singh, D. P., and B. B. Singh, 2011: Breeding for tolerance to abioticstresses in mungbean. J. Food Legumes 24, 83—90.

Singh, K. B., R. S. Malhotra, and M. C. Saxena, 1989: Chickpea eval-uation for cold tolerance under field condition. Crop Sci. 29, 282—285.

Singh, K. B., R. S. Malhotra, and M. C. Saxena, 1990: Source of toler-ance to cold in Cicer sp. Crop Sci. 30, 1136—1138.

Singh, K. B., M. Omar, M. C. Saxena, and C. Johanson, 1996: Registra-tion of FLIP 87-59C, a drought tolerance chickpea germplasm line.Crop Sci. 36, 472.

Singh, K. B., M. Omar, M. C. Saxena, and C. Johansen, 1997: Screeningfor drought resistance in spring chickpea in the mediterranean region.J. Agron. Crop Sci. 178, 227—235.

Singh, A. K., R. A. Singh, and S. G. Sharma, 2001: Influence of salinityon activity of hydrolytic and oxidative enzymes in chickpea seedlings.Indian J. Plant Physiol 6, 84—86.

Singha, P., J. Bhowmick, and B. K. Chaudhury, 2006: Effect of tempera-ture on yield and yield components of fourteen wheat (Triticum aes-tivum L.) genotypes. Environ. Ecol. 24, 550—554.

Singla, R., and N. Garg, 2005: Influence of salinity on growth and yieldattributes in chickpea. Turk J. Agric. For. 29, 231—235.

Slemi, N., M. Lachaal, C. Andelly, A. Soltani, and M. Hajji, 2001: Phys-iological behaviour of two chickpea Tunisian varieties irrigated withsaline nutrient solution. Dev. Plant Soil Sci. 92, 408—409.

Sohrabi, Y., G. Heidari, and B. Esmailpoor, 2008: Effect of salinity ongrowth and yield of Desi and Kabuli chickpea Cultivar. Pak. J. Biol.Sci. 11, 664—667.

Srinivasan, A., H. Takeda, and T. Senboku, 1996: Heat tolerance in foodlegumes as evaluated by cell membrane thermo stability and chloro-phyll fluorescence techniques. Euphytica 88, 35—45.

Srinivasan, A., C. Johansen, and N. P. Saxena, 1998: Cold tolerance dur-ing early reproductive growth of chickpea (Cicer arietinum L.): char-acterization of stress and genetic variation in pod set. Field Crops Res.57, 181—193.

Srinivasan, A., N. P. Saxena, and C. Johansen, 1999: Cold tolerance dur-ing early reproductive growth of chickpea (Cicer arietinum L.):genetic variation in gamete development and function. Field CropsRes. 60, 209—222.

Stamp, P., 1994: Marker-Assisted Breeding. In: Proceedings of the IXMeeting of EUCARPIA section on Biometrics in plant breeding, Wa-geningen, the Netherlands, pp. 32—44.

Steponkus, P. L., M. Uemura, and M. S. Webb, 1993: A contrast of thecryostability of the plasma membrane of winter rye and spring oat-two species that widely differ in their freezing tolerance and plasmamembrane lipid composition. In: P. L. Steponkus (ed.), Advances inLow Temperature Biology, 211—312. JAI Press, London.

Subbarao, G. V., C. Johansen, A. E. Slinkard, R. C. N. Rao, N. P.Saxena, and Y. S. Chauhan, 1995: Strategies for improving droughtresistance in grain legumes. CRC Crit. Rev. Plant Sci. 14,469—523.

Sullivan, C. Y., 1972: Mechanisms of heat and drought resistance ingrain sorghum and methods of measurements. In: N. G. P. Rao, andR. L. House (eds), Sorghum in the Seventie, 247—264. Oxford &IBH Publishing Co., New Delhi, India.

Summerfield, R. J., and H. C. Wein, 1980: Effects of photoperiod andair temperature on growth and yield of economic legumes. In: R. J.Summerfield, and A. H. Bunting (eds), Advances in Legumes Science.Volume1 of the Proceedings of the International Legumes Conference,17—36. Kew, UK.

Summerfield, R. J., P. Hadley, E. H. Roberts, F. R. Minchin, and S.Rawsthrone, 1984: Sensitivity of chickpea (Cicer arietinum L.) tohot temperatures during the reproductive period. Exp. Agric. 20,77—93.

Summerfield, R. J., S. M. Virmani, E. H. Roberts, and R. H. Ellis, 1990:Adaption of chickpea to agroclimatic constraints. In: H. A. van Rhee-nen, and M. C. Saxena (eds), ‘Chickpea in the Nineties. Proceedingsof the Second International Workshop on Chickpea Improvement’. 4–8December 1989. ICRISAT Center, Hyderabad, AP, India, 50—61.ICRISAT Publishing, Hyderabad, India.

Swaraj, K., and N. R. Bishnoi, 1999: Effect of salt stress on nodulationand nitrogen fixation in legumes. Indian J. Exp. Biol. 37, 843—848.

Syvanen, A. C., 2005: Toward genome-wide SNP genotyping. Nat.Genet. 37, S5—S10.

Tanksley, S. D., and J. C. Nelson, 1996: Advanced backcross QTLanalysis: a method of the simultaneous discovery and transfer of valu-able QTLs from unadapted germplasm into elite breeding lines. Theor.Appl. Genet. 92, 191—203.

Tasaka, Y., I. Nishida, S. Higashi, T. Beppu, and N. Muratu, 1990: Fattyacid composition of phosphatidglyserols in relation to chilling sensitiv-ity of woody plants. Plant Cell Physiol. 31, 545—550.

Tejera, N. A., M. Soussi, and C. Liuch, 2006: Physiological and nutri-tional indicators of tolerance to salinity in chickpea plants growingunder symbiotic conditions. Environ. Exp. Bot. 58, 17—24.

Tester, M., and P. Langridge, 2010: Breeding technologies to increase incrop production in changing world. Science 327, 818—822.

Toker, C., and M. I. Cagirgan, 1998: Assessment of response to droughtstress of chickpea (Cicer arietinum L.) lines under rainfed conditions.Tr. J. Agric. For. 22, 615—621.

Toker, C., C. Lluch, N. A. Tejera, R. Serraj, and K. H. M. Siddique,2007a: Abiotic stress. In: S. S. Yadav, R. Redden, W. Chen, and B.Sharma (eds), Chickpea Breeding and Management, 474—496. CABInternational, UK.

Toker, C., H. Canci, and T. Yildirim, 2007b: Evaluation of perennialwild Cicer species for drought resistance. Genet. Resour. Crop Evol.54, 1781—1786.

Tuberosa, R., and S. Salvi, 2006: Genomic approaches to improvedrought tolerance in crops. Trends Plant Sci. 11, 405—412.

Turner, N. C., 1986: Crop water deficit: a decade of progress. Adv.Agron. 39, 1—51.

Turner, N. C., and B. R. Whan, 1995: Strategies for increasing produc-tivity from water limited areas through genetic means. In: B. Sharma,V. P. Kulshreshtra, N. gupta, and S. K. Mishra (eds). GeneticResearch and Education: Current Trends and the Next Fifty years, 545—557. Indian society of Genetics and Plant Breeding, New Delhi,India.

Turner, N. C., S. Abbo, J. D. Berger, S. K. Chaturvedi, R. J. French, C.Ludwig, D. M. Mannur, S. J. Singh, and H. S. Yadava, 2007: Osmotic


adjustment in chickpea (Cicer arietinum L.) results in no yield benefitunder terminal drought. J. Exp. Bot. 58, 187—194.

Turner, N. C., T. D. Colmer, J. Quealy, R. Pushpavalli, L. Krishnamur-thy, J. Kaur, G. Singh, K. H. M. Siddique, and V. Vadez, 2013: Salin-ity tolerance and ion accumulation in chickpea (Cicer arietinum L.)subjected to salt stress. Plant Soil 365, 347—361.

Tyagi, P. K., R. K. Pannu, K. D. Sharma, B. D. Chaudhary, and D. P.Singh, 2003: Response of different wheat (Triticum aestivumL.) culti-vars to terminal heat stress. TAC 24, 20—21.

Ulemale, C. S., S. N. Mate, and D. V. Deshmukh, 2013: Physiologicalindices for drought tolerance in chickpea (Cicer arietinum L.). WorldJ. Agric. Sci. 9, 123—131.

Upadhyaya, H. D., N. Dronavalli, C. L. L. Gowda, and S. Singh, 2011:Identification and evaluation of chickpea germplasm for tolerance toheat stress. Crop Sci. 51, 2079—2094.

Upadhyaya, H. D., J. Kashiwagi, R. K. Varshney, P. M. Gaur, K. B.Saxena, L. Krishnamurthy, C. L. L. Gowda, R. P. S. Pundir, S. K.Chaturvedi, P. S. Basu, and I. P. Singh, 2012: Phenotyping chickpeasand pigeonpeas for adaptation to drought. Front. Physiol. 3, 1—10.

Vadez, V., L. Krishnamurthy, R. Serraj, P. M. Gaur, H. D. Upadhyaya,D. A. Hoisington, R. K. Varshney, N. C. Turner, and K. H. M. Siddi-que, 2007: Large variation in salinity tolerance in chickpea isexplained by differences in sensitivity at the reproductive stage. FieldCrops Res. 104, 123—129.

Vadez, V., M. Rashmi, K. Mithila, R. Muralidharan, R. Pushpavalli, N.C. Turner, L. Krishnamurthy, P. M. Gaur, and D. C. Timothy, 2012a:Large number of flowers and tertiary branches, and higher reproduc-tive success increase yields under salt stress in chickpea. Eur. J.Agron. 41, 42—51.

Vadez, V., L. Krishnamurthy, M. Thudi, C. Anuradha, T. D. Colmer, N.C. Turner, K. H. M. Siddique, P. M. Gaur, and R. K. Varshney,2012b: Assessment of ICCV 2 9 JG 62 chickpea progenies showssensitivity of reproduction to salt stress and reveals QTL for seed yieldand yield components. Mol. Bred. 30, 9—21.

Varshney, R. K., and A. Dubey, 2009: Novel genomic tools and moderngenetic and breeding approaches for crop improvement. J. Plant Bio-chem. Biotechnol. 18, 127—138.

Varshney, R. K., P. J. Hiremath, P. Lekha, J. Kashiwagi, J. Balaji, A. A.Deokar, V. Vadez, Y. Xio, R. Srinivasan, P. M. Gaur, K. H. M. Siddi-que, C. D. Town, and D. A. Hoisington, 2009: A comprehensiveresource of drought- and salinity- responsive ESTs for gene discoveryand marker development in chickpea (Cicer arietinum L.). BMCGenomics 10, 523.

Varshney, R. K., K. C. Bansal, P. K. Aggarwal, S. K. Dutta, and P. Q.Craufurd, 2011: Agricultural Biotechnology for crop improvement in avariable climate: hope or hype? Trends Plant Sci. 16, 363—371.

Varshney, R. K., M. Thudi, S. N. Nayak, P. M. Gaur, J. Kashiwagi, L.Krishnamurthy, D. Jaganathan, J. Koppolu, A. Bohra, S. Tripathi, A.Rathore, A. K. Jukanti, V. Jayalakshmi, A. Vemula, S. Singh, M. Ya-sin, M. S. Sheshshayee, and K. P. Viswanatha, 2013a: Genetic dissec-tion of drought tolerance in chickpea (Cicer arietinum L.). Theor.Appl. Genet., DOI: 10.1007/s00122-013-2230-6.

Varshney, R. K., J. M. Ribaut, E. S. Buckler, R. Tuberosa, J. A. Rafal-ski, and P. Langridge, 2013b: Can genomics boost productivity oforphan crops. Nat. Biotechnol., 30, 1172—1176, 2012.

Varshney, R. K., P. M. Gaur, S. K. Chamarthi, L. Krishnamurthy, S. Tri-pathi, J. Kashiwagi, V. K. Singh, M. Thudi, and D. Jaganathan,2013c: Fast-track introgression of “QTL-hotspot” for root traits andother drought tolerance trait in JG 11, an elite and leading variety ofchickpea (Cicer arietinum L.). Plant Genome., DOI: 10.3835/plantge-nome2013.07.0022.

Varshney, R. K., S. M. Mohan, P. M. Gaur, N. V. P. R. Gangarao, M.P. Pandey, A. Bohra, S. L. Sawargaonkar, A. Chitikineni, P. K.Kimurto, P. Janila, K. B. Saxena, A. Fikre, M. Sharma, A. Rathore,A. Pratap, S. Tripathi, S. Dutta, S. K. Chaturvedi, N. Mallikarjuna, G.Anuradha, A. Babbar, A. K. Choudhary, M. B. Mhase, C. H. Bharad-waj, D. M. Mannur, P. N. Harer, B. Guo, X. Liang, N. Nadarajan, andC. L. Gowda, 2013d: Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Bio-technol. Adv. 31, 1120—1134.

Vieira da Silva, J., A. W. Naylor, and J. Kramer, 1974: Some ultrastruc-tural and enzymatic effects of water stress in cotton (Gossypium L.)leaves. Proc. Nat. Acad. Sci. USA 71, 3243—3247.

Vij, S., and A. K. Tyagi, 2007: Emerging trends in the functional ge-nomics of the abiotic stress response in crop plants. Plant Biotechnol.J. 5, 361—380.

Wahid, A., S. Gelani, M. Ashraf, and M. R. Foolad, 2007: Heat toler-ance in plants: an overview. Environ. Exp. Bot. 61, 199—223.

Wang, J., Y. T. Gan, F. Clarke, and C. L. McDonald, 2006: Response ofchickpea yield to high temperature stress during reproductive develop-ment. Crop Sci. 46, 2171—2178.

Wang, X., Y. Liu, Y. Jia, H. Gu, H. Ma, T. Yu, H. Zhang, Q. Chen, L.Ma, A. Gu, J. Zhang, S. Shi, and H. Ma, 2012: Transcriptionalresponses to drought stress in root and leaf of chickpea seedling. Mol.Biol. Rep. 39, 8147—8158.

Wery, J., 1990: Adaptation to frost and drought stress in chickpea andimplications in plant breeding. Option Mediterraneennes-Serie Semi-naires-n.o 9, 77—85.

Xu, Q., A. Q. Paulsen, J. A. Guikema, and G. M. Paulsen, 1995: Func-tional and ultrastructural injury to photosynthesis in wheat by hightemperature during maturation. Environ. Exp. Bot. 35, 43—54.

Yordanov, I., V. Velikova, and T. Tsonev, 2003: Plant Responses todrought and stress. Bulg. J. Plant Physiol. (Special issue), 187—206.

Zaman-Allah, M., D. M. Jenkinson, and V. Vadez, 2011a: A conserva-tive pattern of water use, rather than deep or profuse rooting, is criticalfor the terminal drought tolerance of chickpea. J. Exp. Bot. 62,4239—4252.

Zaman-Allah, M., D. M. Jenkinson, and V. Vadez, 2011b: Chickpea gen-otrypes contrasting for seed yield under terminal drought stress in thefield differ for traits related to the control of water use. Funct. PlantBiol. 38, 270—281.

Zamir, D., 2001: Improving plant breeding with exotic genetic libraries.Nat. Rev. Genet. 2, 983—989.


Review Abiotic stresses, constraints and improvement ... · molecular breeding (MB) approaches...

Documents

Transcript of Review Abiotic stresses, constraints and improvement ... · molecular breeding (MB) approaches...