8 abiotic stresses, constraints and improvement strategies in chickpea

Plant Breeding 133, 163–178 (2014) © 2014 Blackwell Verlag GmbH doi:10.1111/pbr.12150 Review Abiotic stresses, constraints and improvement strategies in chickpea U D A Y C J H A 1, S U S H I L K C H A T U R V E D I 1, A B H I S H E K B O H R A 1, P A R T H A S B A S U 1, M U H A M M A D S K H A N and D E B M A L Y A B A R H 3,4 Indian Institute of Pulses Research (IIPR), Kanpur, 208024, Uttar Pradesh India; 2Centre for Agricultural Biochemistry and Biotechnology, University of Agriculture, Faisalabad, Pakistan; 3Centre for Genomics and Applied Gene Technology, Institute of Integrative Omics and Applied Biotechnology (IIOAB), Nonakuri, Purba Medinipur, West Bengal 721172, India; 4Corresponding author, E-mail: dr.barh@gmail.com With figure and tables Received June 6, 2013/Accepted November 23, 2013 Communicated by R Varshney Abstract Chickpea (Cicer arietinum L.) is cultivated mostly in the arid and semiarid regions of the world Climate change will bring new production scenarios as the entire growing area in Indo–Pak subcontinent, major producing area of chickpea, is expected to undergo ecological change, warranting strategic planning for crop breeding and husbandry Conventional breeding has produced several high-yielding chickpea genotypes without 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 of chickpea The genetic complexity of these abiotic stresses and lack of proper screening techniques and phenotyping techniques and genotypeby-environment interaction have further jeopardized the breeding programme of chickpea Therefore, considering all dispiriting aspects of abiotic stresses, the scientists have to understand the knowledge gap involving the physiological, biochemical and molecular complex network of abiotic stresses mechanism Above all emerging ‘omics’ approaches will lead the breeders to mine the ‘treasuring genes’ from wild donors and tailor a genotype harbouring ‘climate resilient’ genes to mitigate the challenges in chickpea production Key words: Chickpea breeding — cold stress — drought tolerance — salinity stress — QTLs Globally, chickpea (Cicer arietinum L.) is the second most important legume crop after dry beans (Varshney et al 2013b) According to FAOSTAT data (2012), chickpea is grown in 54 countries with nearly 90% of its area covered in developing countries (Gaur et al 2012) Notably, almost 80% of global chickpea is produced in Southern and South-Eastern Asia and India ranks first in the world, contributing 68% of the global chickpea production accompanied by Australia (60%), Turkey (47%), Myanmar (42%) and Ethiopia (35%) (FAOSTAT 2012, Gaur et al 2012) Worldwide chickpea production is estimated to be 11.30 million tons from 12.14 million area with an average productivity of 931 kg/ha (FAOSTAT 2012) In India, it tops the list of pulse crops and is cultivated in 8.32 million ha, producing a total of 7.70 million tons with an average yield of 925.5 kg/ha (FAOSTAT 2012) From the nutrition perspective, chickpea seed contains 20–30% crude protein, 40% carbohydrate, and 3–6% oil (Gil et al 1996) Besides, pulses supplemented diets are also good source of calcium, magnesium, potassium, phosphorus, iron and zinc (Ibrikci et al 2003) Chickpea faces various abiotic stresses during its life cycle such as drought, cold, terminal heat and salinity (Ryan 1997, Millan et al 2006), and it also encounters water logging, acidity and metal toxicity stresses The yield losses due to abiotic stresses may exceed (6.4 million tons) those caused by biotic stresses (4.8 million tons) (Ryan 1997) Substantial economic losses of 1.3 billion, 186 million and 354 million US dollars due to drought/heat, cold and salinity, respectively, have raised tremendous concerns among the chickpea-growing countries (Ryan 1997) Given the complex genetic architecture and unpredictable occurrence, breeding against abiotic stresses has always been a challenging task Further, drastic climate changes have caused phenotypic plasticity implying changes in phenotype of plant (Nicotra et al 2010), and this phenotypic plasticity permits to adjust their form and function according to the change of resource and habitat (Magyar et al 2007) Tolerance to abiotic stresses exhibits complex quantitative inheritance that is also influenced by a number of genetic and environmental interactions As an obvious reason, these strong genotype-by-environment (G E) interactions have also posed impediments in breeding against these stresses An exhaustive search of germplasm for appropriate donors to these stresses represents the foremost step in breeding for stress tolerance Given the context, a detailed list of the genotypes showing tolerance to various abiotic stresses has been presented in Table 1, which can be used as potent resistant/tolerant sources for introgressing the quantitative trait loci (QTLs) governing stress tolerance to susceptible varieties This review article summarizes the negative impacts and constraints of major abiotic stresses on chickpea yield along with providing a critical appraisal of various conventional breeding strategies Additionally, this article also provides an overview on recent developments of genomic resources and various molecular breeding (MB) approaches including marker-assisted backcrossing (MABC), marker-assisted recurrent selection (MARS), which may act as powerful supplement to conventional breeding particularly in the context of abiotic stresses Drought Stress Background constraints and its effects Drought is one of the most important abiotic stresses, which limits production in different parts of the world and has remained the 164 U C JHA, S K CHATURVEDI, A BOHRA et al Table 1: Sources of resistance to various abiotic stresses and their basis of tolerance in chickpea Abiotic stress Drought tolerance H208, H355, S26, G24, RS10, RS11 and Azerbaijan 583 ICC4958 – Deep rooting, 30% more root volume and mass than cultivated genotypes FLIP 87-59C ICC96029 FLIP92-154C ICCV2 ICCV93032, ICCV94008, ICCV90033 and ICC89204 ICC5680, ICC10448 RILs from ICC4958 Annegiri ILC1799, ILC3832, FLIP98-141, ILC3182, FLIP98-142C, ILC3101 and ILC588 ICC8261 Beja and Kesseb ICC4958, ICC8261 – Early flowering – Early flowering – Small leaf and leaf area Prolific rooting and deep rooting trait Escape through earliness ACC316 and ACC317 ICC13124 HC-5 and H02-36 MCC544, MCC696 and MCC693 ILC482 ICC7571 Terminal Heat stress ILC482, Annegiri, ICCV10 ICCV88512 and ICCV88513 ACC316and ACC317 ICC1205 ICC456, ICC637, ICC1205, ICC3362, ICC3761, ICC4495, ICC4958, ICC4991, ICC6279, ICC6874, ICC7441, ICC8950, ICC11944, ICC12155, ICC14402, ICC14778, ICC14815, ICC15618 ICC14346 ICCV92944 ICC1205 and ICC15614 ICC14778 Freezing tolerance Azerbaijan, ILC482 ILC-794, ILC-1071, ILC1251, ILC1256, ILC1444, ILC1455, ILC1464, ILC1875, ILC3465, ILC3598, ILC3746, ILC3747 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 ICCV 88502, ICCV88503 ICCV96029, ICCV96030 Salinity tolerance Underlying mechanism/physiological and biochemical basis for tolerance Tolerant sources ICCV88516 Sonali and Rupali MCC426 and MCC252 L550 ICCC32 and 1CCL86446 CSG88101, CSG8927 Amdoun l FLIP.98-74, FLIP.87-59, FLIP.87-85, and ILC 3279 SG-11 and DHG-84-11 CSG8962 and ICCV96836 CSG9651 ILC1919 CM88 ICC5003, ICC15610 and ICC1431 Hahshem JG62 Avoidance through root traits Lower nodule mortality Root length density and root dry weight Early flowering(escape mechanism) Root length, root weight and root volume Rooting depth and root biomass Mesophyll resistance and proline accumulation Higher proline content Harvest index and rate of partitioning positively associated with (DRI) Cell membrane stability – Early flowering Pollen germination and tube growth Early flowering, seed yield at maturity Early maturing Early maturity High pod no; filled pods/plant under heat stress High rate of partitioning, cooler canopy temp Extract maximum soil water References Saxena and Singh (1987) Saxena et al (1993), Krishnamurthy et al (2003) and Kashiwagi et al (2005, 2006a) Singh et al (1996) Kumar and Rao (1996) Toker and Cagirgan (1998) Kumar and Abbo (2001) Kanouni et al (2002) Saxena (2003) Serraj et al (2004a) Sabaghpour et al (2006) Gaur et al (2008) Labidi et al (2009) Kashiwagi et al (2008) Canci and Toker (2009) Parmeshwarappa et al (2010) Kumar et al (2010a) Mafekheri et al (2010) Mafakheri et al (2011) Kashiwagi et al (2013) Srinivasan et al (1996) Dua (2001) Canci and Toker (2009) Devasirvatham et al (2010) Krishnamurthy et al (2011) – – Upadhyaya et al (2011) Gaur et al (2012) Devasirvatham et al (2012, 2013) Kashiwagi et al (2008), Zaman-Allah et al (2011a,b) and Krishnamurthy et al (2013a) Saxena and Singh (1987) Singh et al (1989) – Wery (1990) Pod set at cold temperature(tolerance/ resistance) Earliness(escape mechanism) Srinivasan et al (1998, 1999) Sandhu et al (2002) and Kumar and Rao (1996) Clarke and Siddique (2003) Clarke et al (2004) Nezami et al (2007) Lauter and Munns 1986 Dua (1992) Dua and Sharma (1995) – Pollen selection at low temperature – Physiological – Lower Na+ in root, that is, exclusion of Na+ Protection of photosynthetic organ from attack of Na+ by retaining Na+ in root and supply of K+ to shoot Physiological Physiological – – Physiological Biochemical Higher yield under salinity – Higher yield under salinity, Early flowering Slemi et al (2001) Bruggeman et al (2003) Singh et al (2001) and Singh (2004) Maliro et al (2004) Singla and Garg (2005) Tejera et al (2006) Sarwar et al (2006) Vadez et al (2007) Sohrabi et al (2008) Vadez et al (2007, 2012b) Stress breeding in chickpea most recalcitrant when attempted to address through traditional breeding approaches (Tuberosa and Salvi 2006, Toker et al 2007a) It is important to note that the water scarcity alone causes 70% of agricultural yield loss across the globe (Boyer 1982) Moreover, in concern with drought, desiccation has been reported as the most severe form of drought that leads to loss of protoplasmic water (Yordanov et al 2003) Drought imposes negative effects on plant growth and development by impeding lipid biosynthesis and lowering the membrane lipid, which ultimately results 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 process of photosynthesis and other metabolic activity of plant (Chaves 1991, Chaves et al 2003, 2009, Pinheiro and Chaves 2011) Notably, almost 90% of chickpea is grown under rainfed conditions (Kumar and Abbo 2001) where terminal drought limits its productivity (Toker et al 2007a) The result of drought relies upon the water-holding capacity, evapo-transpiration and need of water for crop plants (Toker et al 2007a) Drought accounts for 40–45% yield losses in chickpea across the globe (Ahmad et al 2005) Strategy for drought acclimation Harnessing genetic variability, genetic basis and breeding for drought tolerance To a large extent, success of any crop-improvement programme is determined by the quantum of exploitable genetic variation that exits in the crop germplasm Keeping the above in view, a large number of accessions have been routinely screened for various traits specifically to incorporate drought tolerance in chickpea For instance, a preliminary study conducted during 1992 to 1995 at Tel Hayda (northern Syria) using 4165 lines by establishing the proper screening and rating scale (1–9), and subsequently, a total of 19 drought resistant lines were identified (Singh et al 1997) In a similar manner, 64 chickpea lines were evaluated under rainfed conditions for drought tolerance showed 53% yield advantage of the mentioned lines under non-stressed conditions compared with stress conditions (Toker and Cagirgan 1998) Likewise, a set of 24 genotypes was screened considering five important indices, viz drought response index (DRI), stress tolerance index (STI), tolerance (TOL), mean productivity (MP) and geometric mean productivity (GMP), which were recorded under two different moisture levels at two different sowing times STI and MP were chosen as the best indices for evaluation of drought resistance (Kanouni et al 2002), and similarly, Pouresmael et al (2013) reported STI as 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 the process of crop domestication and selection, these natural reservoirs of immense genetic variation have gone unnoticed (Zamir 2001) In regard to chickpea, perennial wild Cicer species, viz C anatolicum, C microphyllum, C montbretti, C oxydon and C songaricum, were evaluated for drought tolerance, using a scale of (highly tolerant) to (highly susceptible) (Toker et al 2007b) Taken into consideration the drought tolerance index (DTI), a mini-core collection comprising 211 chickpea accessions was screened for three consecutive years The study revealed 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 tolerant, 78 as tolerant, 74 as moderately tolerant, 39 as sensitive and 20 as highly sensitive (Krishnamurty et al 2010) Similarly 165 from mini-core collection, 10 accessions were identified showing drought tolerance relying on drought susceptible index (DSI) and drought tolerant efficiency per cent (DTE%), tested during 2006–2007 The genotype ICC13124 performed best among the genotypes used and gave maximum yield under irrigated (1220 kg/ha) and rainfed condition (990 kg/ha) (Parmeshwarappa et al 2010) In another instance, screening of 377 accessions using (free from heat and drought stress) to (susceptible to heat and drought) scale led to identification of two genotypes viz ACC316 and ACC317 possessing resistance to drought and heat accompanying least impact of heat and drought on seed weight and having highest heritability (Canci and Toker 2009) To find out the associations of various drought-related traits with DRI, a set of 21 drought-responsive genotypes was tested for two consecutive years and the experimental results demonstrated the positive association of crop growth rate (CGR) with DRI, whereas water-use efficiency (WUE) showed a negative correlation with the DRI (Kashiwagi et al 2013) Moreover, one chickpea landrace (ICC 7571) exhibited a noticeably tolerant reaction against drought across both years Kashiwagi et al 2013 also reported the significant contribution of rate of partitioning or partitioning coefficient (p) towards grain yield under drought conditions, and this observation was also confirmed in another study conducted on a reference collection of chickpea comprising 280 cultivated accessions (Krishnamurthy et al 2013a) Under terminal drought stress, path analysis performed in the reference collection of chickpea exhibited the positive associations of carbon isotope discrimination with harvest index (HI) (Krishnamurthy et al 2013b) In addition to germplasm collections, segregating populations derived from possible combinations of four genotypes viz ICCV 2, A1, ICC 4958 and ICCV 10448 were tested for physiological traits imparting drought tolerance Of the six F2 populations evaluated, highest yield was obtained from progeny sharing ICCV4958 as one of the parent The segregates obtained from A1 ICC 4958, ICCV ICC 4958 explained high seed yield, early and high root mass (Mannur et al 2009) Efforts were also carried out to find out the gene actions underlying drought tolerance using joint scaling test in the cross ‘Hashem’ (cultivar) ICCV 96029, and the investigation elucidated the presence of additive dominance = [j] gene action for grain yield, biological yield and proline content, whereas duplicate epistasis (additive dominance = [j] and dominance dominance = [l] gene action) was observed 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 identified from population ILC 588 ILC 3279, and these QTLs were located on LG3 and LG1 (Rehman et al 2011) More recently, a comprehensive molecular investigation targeting genetic dissection of drought tolerance was carried out in chickpea (Varshney et al 2013a) Two mapping populations namely ICC 4958 ICC 1882 and ICC 283 ICC 8261 were chosen for rigorous phenotypic screening using a variety of drought component traits, which were phenotyped across five different locations in India The phenotypic data along with the genotypic data were subsequently analysed to discover QTLs associated with drought tolerance Importantly, not only main-effect QTLs (45 m-QTLs) but epistatic-QTLs (e-QTLs) were also detected indicating the occurrence of complex genetic interactions controlling drought tolerance In total, the 45 m-QTLs explained almost 60% variance, while 973 e-QTLs accounted upto 90% of the phenotypic variance for various component traits (Varshney et al 2013c) 166 U C JHA, S K CHATURVEDI, A BOHRA et al Table 2: Different QTLs identified for various abiotic stresses in Chickpea Trait Drought tolerance/ avoidance Drought tolerance Mapping population ICC4958 Annigeri ICC8261 ICC283 and ILC 588 ILC 3279 Markers – 97 SSR markers – – – – Drought tolerance ICC4958 Annigeri Salinity tolerance ICCV JG 62 TAA170, ICCM0249, STMS11 and GA24 216 markers ICCV JG 62 – ICCV JG 62 – Identified QTL Linkage group Phenotypic variation (%) References One major QTL contributing root biomass QTLs contributing root traits Two QTL for HI – – – – – 38 Gaur et al (2008) Rehman et al (2011) Four QTL for flowering Three QTL for maturity explaining Three QTL for gs +six QTL for Tc–Ta Two QTL (Q3-1 and Q1-1) – – 45 52 Rehman et al (2011) Rehman et al (2011) – 7–15 Rehman et al (2011) – Rehman et al (2011) – Jaganathan et al (2013) Several QTLs contributing drought tolerance One QTL for seed yield under salinity on Many QTL associated with seed no and 100 seed wt under salinity Many QTL associated with 50% flowering, seed no shoot dry wt LG3 and LG1 LG4 Gaur et al (2008) LG3 19 Vadez et al (2012a) LG 14.8–49.7 Vadez et al (2012a) LG 8.8–37.7 Vadez et al (2012a) gs, Higher stomatal conductance; [Tc–Ta], cooler canopies (canopy temperature minus air temperature); HI, Harvest Index Physiological and biochemical tolerance The plant acclimatizes under drought conditions through different mechanisms like escape, avoidance and tolerance (Levitt 1972, Turner 1986, Loomis and Connor 1992) Drought resistance and its components are almost constantly being redefined (Blum 2005) Drought escape through early phenology Drought escape enables selection of plants completing their life cycle in short period thus making judicious use of available moisture condition (Turner and Whan 1995, Siddique et al 1997) Under terminal drought conditions, early flowering trait provides advantage of avoiding drought and avoids yield loss in chickpea (Subbarao et al 1995, Siddique et al 1999, Kumar and Abbo 2001, Berger 2007) In context of early flowering, a major recessive gene ‘efl-1’ was reported to be responsible for early flowering (Kumar and van Rheenen 2000), and this finding subsequently facilitated the development of super early genotype ICCV 96029 (derived from ICCV ICCV 93929 cross) which flowered within 24 days (Kumar and Rao 1996) at ICRISAT Sabaghpour et al (2006) screened a total of 40 kabuli genotypes and identified ILC1799, ILC3832, FLIP98-141, ILC3182, FLIP98-142C, ILC3101 and ILC588 as superior early genotypes that can escape terminal drought (Table 1) However, selection of genotypes with shorter vegetative period may result in yield penalty (Basu and Singh 2003) Drougth avoidance through root traits Root system of plant imparts drought tolerance through acquiring soil moisture by deep penetration of root, adequate root density and sufficient longitudinal conductance of main roots (Fisher et al 1982) Chickpea genotypes with high root biomass and showing marked drought tolerance have been reported (Brown et al 1989, Saxena et al 1994, Krishnamurthy et al 1996) One of 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 of rooting allows availing the deep soil water in drought conditions (Saxena et al 1993, Krishnamurthy et al 2003 and Kashiwagi et al 2005) Role of deep and prolific rooting trait affecting drought avoidance and yield was examined using ICC4958 ‘Annegiri’ based RIL population consisting of 257 lines However, no significant yield improvement was recorded in this study (Serraj et al 2004a) In addition, the ‘root length density’ (RLD) and maximum ‘root depth’ (RDp) can benefit in drought resistance without affecting yield as assessed in minicore collection of chickpea (Kashiwagi et al 2005) Using 12 chickpea genotypes, a positive association of RLD with seed yield was illustrated at 35 days after sowing (DAS) (Kashiwagi et al 2006a) Notably, genotypes with prolific and deep rooting have been found to be more adapted to drought, but little information is available on the genetic control of root system Taken the above into account, generation mean analysis (GMA) was conducted to estimate the genetic effects of root and shoot traits using six generations (P1, P2, F1, F2, BC1P1 and BC1P2) based on two different crosses viz ICC283 ICC 8261 and ICC4958 ICC1882 The study suggested existence of additive gene action and additive additive gene interactions, which control RLD and root dry weight (RDW) (Kashiwagi et al 2008) In contrast to the destructive method involved in screening of root traits, polyvinyl chloride (PVC) pipes are used making the sampling of root traits easier and efficient in chickpea (Upadhyaya et al 2012) In an investigation aiming at detecting significant QTLs, a major QTL was discovered that controlled one-third of the entire variation for root length and root biomass (Chandra et al 2004) Kumar et al (2010a) investigated the root traits for drought tolerance in six genotypes in both irrigated and rainfed conditions and identified two genotypes viz HC-5 and H02-36 showing high dry matter of roots, high root depth, and high root to shoot ratio, and ultimately, the plant yield advantage However, it has also been observed in some recent studies that profuse and deep rooting not contribute drought Stress breeding in chickpea tolerance in terms of improving yield under drought stress, whereas some moisture preservation traits determine yield improvement under drought in chickpea (Zaman-Allah et al 2011a,b) Tolerance through osmotic adjustment Osmotic adjustment (OA) is an important physiological phenomenon, which controls the water absorption and cell turgor pressure under drought stress (Cattivelli et al 2008) OA confers drought tolerance in many crops of commercial importance like wheat (Blum et al 1999, Morgan 2000), barley (Blum 1989), sorghum (Morgan 1984) In addition to sustaining turgor maintenance during water stress condition (Ali et al 1999), OA also plays a significant role during grain formation under drought stress in wheat (Morgan and Condon 1986) Similarly, several reports have been published in chickpea providing knowledge about the association of OA and yield (Morgan et al 1991, Basu and Singh 2003, Moinuddin and Khanna-Chopra 2004) For example, Serraj and Sinclair (2002) deduced positive role of OA in regard to yield through root development towards higher soil water However, no strong evidence was reported concerning the direct association of OA with yield of plant under drought stress With the progress of water stress, OA enhances progressively witnessed by measuring plant water potential and relative water content (RWC) (Lecoeur et al 1992) By subjecting a set of advanced breeding lines of chickpea to drought stress, variation in OA was recorded for both Indian and Australian conditions No yield advantage was seen under Australian conditions, except the case of early flowering where OA effect exhibited high yield advantage (Turner et al 2007) Similarly, Basu et al (2007) also investigated the genetic difference for OA existing among different chickpea genotypes They also suggested that lowering water potential will reduce the leaf starch content, but soluble sugars hexoses and sucroses get increased, not due to change in OA, suggesting reliability of OA for drought tolerance is not promising in chickpea Water-use efficiency (WUE) is described as amount of biomass produced at the cost of per unit transpired water (Bacon 2004) High WUE is another important criterion while dealing with drought tolerance, and it is calculated by graviometric method in pot culture based on transpiration and yield correlation (Krishnamurthy et al 2007, Upadhyaya et al 2012) A robust screening technique known as carbon isotope discrimination (D13C) was used for measuring WUE in chickpea (Kashiwagi et al 2006b) At different levels of vapour pressure deficit under both field and controlled conditions, some chickpea genotypes displayed low canopy conductance especially at vegetative stage under irrigated conditions and exactly opposite at pod filling stage (Zaman-Allah et al 2011a,b) Based on nodule mortality symptom, inoculating five lines with Mesorhizobium ciceri UPMCa7 and noticing change in N content and root to shoot ratio, loss of chlorophyll, and consequently, the genotypes ‘Beja’ and ‘Kesseb’ were found to be tolerant under drought conditions (Labidi et al 2009) Similarly, antioxidant enzyme activities of ascorbate peroxidase and peroxidase in nodule produced by Mesorhizobium ciceri strains contribute to drought 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 anthesis stage, more accumulation of carbohydrate, catalase (CAT) and peroxidase (POX) was observed in tolerant genotypes indicating the importance of CAT and POX in drought tolerance 167 (Mafakheri et al 2011) With the purpose of identifying some new resistant sources to breed for drought tolerance, the tolerance or susceptibility reactions of 150 Iranian kabuli genotypes were checked under rainfed and irrigated conditions The results obtained were further validated using a pot experiments, and as a consequence, three genotypes MCC544, MCC696 and MCC693 were declared as tolerant to drought stress (Ganjeali et al 2011) The above investigation also confirmed the presence of significant negative correlations between yield and days to flowering under drought conditions Moreover, it also provided emphasis on the fact leaf area can be taken as a decisive factor, while assessing the drought tolerance due to less transpiration in decreased leaf area While evaluating 14 chickpea accessions under moisture and non-moisture environment, three genotypes namely Phule G09103, Phule G 2008-74 and Digvijay were found as drought tolerant which may be due to higher value of drought tolerance efficiency, chlorophyll content, proline content, reduction in drought susceptibility and membrane injury indices (Ulemale et al 2013) Other crucial physiological parameters viz., photochemical efficiency of PII system, RWC, SPAD chlorophyll metre reading, cell membrane integrity and stomatal conductance contributing to drought tolerance have also been investigated in chickpea (Pouresmael et al 2013) Terminal Heat Stress Background constraints and its effects Concerning heat stress, Wahid et al (2007) reported that the rise in temperature beyond certain optimum level is detrimental to the crop growth causing severe injuries that are collectively termed as ‘heat stress’ Impact of high temperature on plant growth has been reported on various legume crops including dry bean (Prasad et al 2002), groundnut (Prasad et al 2003) and soybean (Baker et al 1989) However, a significant progress has not been achieved in regard to the effect of heat on different morphological and physiological stages of chickpea (Wang et al 2006) Being a cool season crop, chickpea is also susceptible to high temperature (30–35°) for few days at flowering stage and can cause substantial yield loss (Summerfield and Wein 1980, Saxena et al 1988) Summerfield et al (1984) found the negative relationship between the effect of high temperature at reproductive phase and yield in chickpea Evolution or more precisely the domestication of chickpea has enforced the selection of various phenological changes in accordance with the changes of habitats (Berger et al 2011) In the Mediterranean region, chickpea 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 vegetative stage and 20–27°C and even >30°C temperature during reproductive stage (Summerfield et al 1984, 1990, Berger and Turner 2007) Exposure of various chickpea genotypes beyond 35°C temperature shows no pod setting (Basu et al 2009) The preanthesis and anthesis stages are the stages that are most vulnerable to high temperature stress (Devasirvatham et al 2013) High temperature hampers photosynthesis by damaging both structural and functional activity of chlorophyll and lowers the chlorophyll content (Xu et al 1995) Temperature beyond 40°C causes disruption in photo system I and II (Baker 1991, Sharkey 2005) and also affects respiration (Kurets and Popov 1988), membrane composition and its stability (Levitt 1969), nitrogen 168 fixation (Black et al 1978) and water relation (McDonald and Paulsen 1997) High temperature stress exerts pronounced effect on reproductive phase, which leads to impairment in pre-anthesis, postanthesis and fertilization processes ultimately resulting in loss of seed weight and yield (Nakano et al 1997, 1998, Prasad et al 2003, Upadhyaya et al 2011) In chickpea, high temperature stress also causes reduction in number of flowers, pollen production, 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 is more than stigma, and this observation has been confirmed both in field as well as under controlled conditions using genotypes like ICC1205/ICC15614 (heat tolerant) and ICC 4567/ICC10685 (sensitive) (Devasirvatham et al 2012, 2013) Heat stress marks noticeable effects in anther locule number, anther epidermis wall thickening and pollen sterility (Devasirvatham et al 2013) For instance, when ICC 5912 was kept at 35/20°C for 24 h before anthesis, the genotype became sterile, whereas the other genotype ICCV92944 produced fertile pollens (Devasirvatham et al 2010) Strategy for heat acclimation Harnessing genetic variability, genetic basis and breeding for heat tolerance Germplasm variability for heat tolerance is inevitable for developing a genotype with heat tolerance Dua (2001) documented two genotypes ICCV 88512 and ICCV 88513 exhibiting heat tolerance Another chickpea genotype ICCV 92944 was declared as heat tolerant in field condition (Gaur et al 2010) and subsequently released as cultivar in India (JG14) and Myanmar (Yezin 6) (Gaur et al 2012) Furthermore, while screening the reference collection (280 accessions) at two locations in India (Patancheru and Kanpur), three genotypes ICC3362, ICC6874 and ICC12155 were shown as heat tolerant based on the criterion ‘heat tolerance index’ (HTI) (Krishnamurthy et al 2011) Similarly, a promising heat-tolerant line ‘ICC14346’ was recovered through the 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, Devasirvatham et al (2012, 2013) registered two chickpea genotypes ICC1205 and ICC15614 as heat-tolerant lines Notwithstanding the immense importance of heat tolerance, extensive studies have not been carried out to discover the inheritance patterns of heat tolerance in chickpea However, recently Upadhyaya et al (2011) suggested that heat tolerance in chickpea is under the control of multigenes As an alternative to direct selection of the heat-tolerant genotypes, choice of early flowering and maturity genotypes can be made, thereby bypassing cumbersome phenotyping for heat stress in Mediterranean spring sown and south Indian 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 (Sullivan 1972), which is evident from various reports available from different legumes including chickpea (Srinivasan et al 1996) Other factors like lipid composition and heat shock protein accumulation in the pollen can also assist in identification of heat-tolerant genotypes (Blum 1988) Besides, osmoregulator contents can also provide defiance against heat stress (Evan and Malmberg 1989, Flores 1991) Importantly, the external application of abscisic acid (ABA) can protect plant from heat stress by inducing other osmolytes viz., proline, glycine betaine and trehalose (Kumar et al 2012) Electrolyte leakage and fluo- U C JHA, S K CHATURVEDI, A BOHRA et al rescence tests can aid in screening for heat stress (Srinivasan et al 1996) Additionally, as reported in some cereal crops like wheat, high grain filling rate and high grain weight under heat stress condition can also act as crucial selection criteria for heat tolerance (Tyagi et al 2003, Singha et al 2006, Dias and Lidon 2009) Similarly, in case of chickpea, pod filling rate and high 100-seed weight can be important selection parameters for heat tolerance Nevertheless, Fokar et al (1998) suggested some other important standards to assess heat tolerance like stay green character and retention of chlorophyll under heat stress In the current scenario of rising global temperature, screening of pollen viability and pollen-based screening techniques under high temperature can be particularly beneficial for elevating the levels of heat tolerance in chickpea genotypes (Devasirvatham et al 2012) Low Temperature Stress Background constraints and its effects Cold temperature stress represents a major limiting factor in chickpea production especially in North India, Canada and some parts of Australia Based on the severity of cold, low temperature injury can be classified into two types: (i) chilling injury when 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 pollen germination Moreover, it adversely affects photosynthesis (Bell 1993), electron transport (Hallgren and Oquest 1990) and enzymes involved in CO2 fixation (Sassenrath et al 1990) Due to 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 tolerance mechanism involves a series of biochemical and physiological changes that cause increase in ABA (Rikin and Richmond 1976, Ciardi et al 1997, Morgan and Drew 1997), alteration in lipid composition in cell membrane (Graham and Patterson 1982, Murata 1983, Tasaka et al 1990) and also the changes in osmolytes and increase in antioxidants (Fridovich 1986, Halliwell and Gutteridge 1989) Low temperature stress is becoming more prevalent in temperate region creating a serious threat to vegetative growth by several means like creating chlorosis, necrosis of leaf tip and curling of whole leaf Similarly, reproductive stage represents the most vulnerable phase within where plenty of damaging 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 seed quality and seed yield (Kumar et al 2007, 2010b) The harmful effect of low temperature (below 15°C) is reported from various chickpea-growing areas like Australia (Siddique and Sedgley 1986), Mediterranean region (Singh 1993), India (Savithri et al 1980, Srinivasan et al 1998) and even within controlled laboratory conditions (Srinivasan et al 1999, Clarke et al 2004, Nayyar et al 2005) Strategy for low temperature tolerance acclimation Harnessing genetic variability, genetic basis and breeding for low temperature tolerance Identification of cold tolerant chickpea in Mediterranean region poses the essential prerequisite for enhancing yield during winter sowing, both at freezing (below À1.5°C) and chilling (À1.5 to Stress breeding in chickpea 15°C) temperatures, which affects the entire crop development process starting from germination to maturity (Croser et al 2003) Phenological stage should be taken under consideration for assessing the cold tolerance of a genotype from germination to flowering stage To ascertain the sowing date for freezing resistance, 29 genotypes were screened at five locations at two severe winter (À10°C to À18°C) temperatures, as a result FLIP 81-293C, FLIP 82-127C and FLIP82-128C offered resistance to low temperatures (Wery 1990) In regard to the number of genes underlying tolerance, the genetics of cold tolerance was elucidated by Malhotra and Singh (1991) They considered six different crosses for applying combining ability and GMA, and consequently, the presence of additive additive and dominance dominance interactions with duplicate epitasis was revealed Furthermore, the inheritance analysis also demonstrated that tolerance to cold is dominant over susceptibility Considering pollen as vital component in manipulating the chilling tolerance, selections for pollen at gametophytic stage practiced in chickpea and flower colour was chosen as an effective visible marker during the selection of genotypes (Clarke et al 2004) Alternatively, mutation breeding has also appeared as promising way to creating freezing stress tolerant genotypes in chickpea (Akhar et al 2011) Use of gamma rays as a potent mutagen to induce mutation was manifested in three chickpea genotypes at different doses, that is, 60, 100, 140 and 180 Gy of gamma rays and keeping the shoots at LT50 (50% of lethal temperature) The two genotypes MCC741 and MCC495 showed the highest survival of 80.1% and 64.6% at 180 and 140 Gy doses, respectively (Akhar et al 2011) With the objective of developing high yielding and low temperature tolerance in cooler region, a panel of 40 genotypes with a susceptible check ILC533 was tested considering different phenological and postharvest trait data for assessing cold tolerance The genotypes showing high tolerance to cold were FLIP95-255C, FLIP93-260C and Sel95TH1716 (Kanouni et al 2009) As another notable observation, morphological traits such as plant height, number of primary branches and number of leaves were found to be more in cold tolerant chickpea genotypes in comparison with sensitive genotypes especially at early stage (30 and 60 DAS) (Chohan and Raina 2011) Annual wild species of chickpea have the potential for freezing tolerance as evident from three C echinospermum and two C reticulatum annual wild chickpea genotypes along with 225 cultivated genotypes of chickpea in both field and controlled condition The most promising wild accessions were ILWC81, ILWC106, ILWC139, ILWC181 and ILWC235, whereas cultivated genotypes exhibiting tolerance were Sel96TH11404, Sel96TH11439, Sel96TH11488, Sel98TH11518, x03TH21 and FLIP93-261C (Saeed et al 2010) Besides lines of C bijugum, ILWC-29/S-10 line of C pinnatifidum and ILWC-35/S-3 line of C echinospermum were reported as resources of freezing tolerance (Singh et al 1990) 169 ABA confers cold tolerance in chickpea involve retention of chlorophyll, greater pollen viability, pollen germination, flower retention and pod set, increase in seed weight and single seeded pod, and decrease in infertile pod in comparison with cold stressed plants Further, ABA also prevents the oxidative damage through enhancing the activities of antioxidants and proline in plant (Kumar et al 2007) Similarly, Bakht et al (2006), illustrated application of exogenous ABA aids in acclimation in frost condition It has also been reported that antioxidative enzymes such as catalase, ascorbate peroxidise, glutathione reductase and sucrose synthase can protect seeds and pod walls from the cold stress and thus can help greatly in developing cold tolerant lines in chickpea (Kaur et al 2009) Salt Stress Background constraints and effects Chickpea production is adversely affected due to salinity in arid and semi-arid regions of world (Ryan 1997, Ali et al 2002) Dua (1992) determined the threshold level of electrical conductivity (EC) of 6dS for survival of chickpea under salinity Salt stress (i) reduces water potential (Hayashi and Murata 1998, Munns 2002, Benlloch-Gonzalez et al 2005), (ii) creates imbalance in ion (Hassanein 2000) and (iii) causes toxicity Salinity also imposes osmotic stress and ion toxicity (Munns 2005), ionimbalance and nutrient deficiency (Tejera et al 2006) in plant Millan et al (2006) discussed the effects of soil salinity on anthocyanin pigmentation in foliages of both desi and kabuli types chickpea In addition to inhibiting growth, photosynthesis, energy and lipid metabolism (Ramoliya et al 2004, Parida and Das 2005), salinity also restrains flower and pod formation (Katerji et al 2001, Vadez et al 2007, 2012a) Sohrabi et al (2008) analysed the effect of sodium (Na) salinity at different levels (0, 3, and 9dSm-1) in kabuli (‘Hashem’ and ‘Jam’) and desi (‘Kaka’ and ‘Pirooz’) genotypes for growth and yield parameter suggested the plant growth, pod number, flower, seed weight and seed number get reduced due to the effect of salinity Moreover, salinity also exerts negative effects on nodulation, nodule size and N2 fixation (Swaraj and Bishnoi 1999, Flowers et al 2010) Interestingly, Samineni et al (2011) declared that both growth stages, that is, vegetative and reproductive are equally sensitive to salinity Strategy for salinity acclimation Like other breeding programmes, breeding for salt tolerance relies on assessment of allelic variation for salt tolerance in the germplasm accompanied by transferring the beneficial allele(s)/ gene(s)/QTLs to the other genetic background to create modern high-yielding cultivars Physiological and biochemical basis of tolerance Harnessing genetic variability, genetic basis and breeding for salinity tolerance As indicated by double bond index (DBI), the external application of abscisic acid (ABA) increases fatty acid desaturation in plasma membrane and results in low cell lysis at low temperature (Bakht et al 2006) Cold stress can be ameliorated by glycine betaine application at budding stage, which improves pollen germination, pollen viability, pollen tube growth, stigma receptivity and ovule viability On the other hand, application at podding stage increases seed yield, number of seeds/pod and RWC (Nayyar et al 2005) The fundamental changes by which external Genetic variation in chickpea genotypes for yield under saline stress was evaluated by several researchers (Sharma et al 1982, Saxena 1984, Flowers et al 2010) Assessment of 160 genotypes of chickpea using 50 mM NaCl or 25 mM Na2So4 salt facilitated identification of the salt tolerant cultivar ‘L550’ and showed that the presence of Na in the shoots checked the normal growth of plant under salinity stress (Lauter and Munns 1986) In another instance, the tolerance of two chickpea genotypes ICCC32 and 1CCL86446 against chloride ion Cl- salinity was demonstrated 170 choosing various yield parameters (Dua 1992) The same way, effects of salinity were tested at germination and seedling stages in 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 retained their tolerance at all salt levels (Al-Mutawa 2003) Likewise, imposing salinity of 0.5, 2, 4, dS/m in six genotypes resulted in comparatively higher production of dry matter by the genotypes FLIP97-74, FLIP87-59 and ILC3279 (Bruggeman et al 2003) Of 252 accessions, 211 mini-core collections of chickpea were examined for salt tolerance, and kabuli types exhibited tolerance to salinity, whereas desi types had susceptibility to salt tolerance (Serraj et al 2004b) Extensive genetic variability for salinity was observed in 200 accessions of chickpea including 19 wild relatives (Maliro et al., 2004) In a similar manner, large degree of variation was also evident in 263 accessions of chickpea mini-core collection, and a positive relationship (r2 = 0.5) was found between seed yields obtained under salinity and nonsalinity conditions The report also suggested that the desi types are more tolerant than kabuli types (Vadez et al 2007) A QTL analysis conducted on population ICCV JG 62 revealed occurrence of significant QTLs for seed yield under saline condition and these QTLs were mapped on linkage group (Vadez et al 2012b) An exhaustive testing for salt tolerance was performed on a sample consisting of landraces and wild relatives from 28 different countries using three different sampling strategies based on scoring of necrosis score and shoot biomass reduction (Maliro et al 2008) Considerable genetic variation for salinity tolerance was noticed among 55 chickpea genotypes that were tested at variable salinity levels, and it was concluded that high pod and seed number bearing genotype which gathers low concentration of salt will provide better tolerance under salinity stress in chickpea (Turner et al 2013) While practicing selection, emphasis should be placed in the direction of constitutive (higher number of flowers) and adaptive traits (higher number of seeds) for salinity tolerance in chickpea (Vadez et al 2012a) Physiological and biochemical basis of tolerance Several physiological parameters such as stomatal conductance, evapo-transpiration and leaf area, and essentially, yield can be chosen as factors for determining the tolerance against salinity (Katerji et al 2003) Another important physiological parameters viz., early maturity, higher predawn water potential, maintenance of high osmotic adjustment and retention of high number of stems per plant can provide tolerance to salinity (Katerji et al 2005) The negative effect of salinity on plant growth was investigated by Singla and Garg (2005), using two desi (CSG8962 and DCP92-3) and two kabuli (CSG9651 and BG267) tested under different salinity levels of 0, 4, and 8/dSm resulting reduction in dry matter of root and shoot and ultimately lowering in productivity CSG9651 performed high tolerance to salinity Ion exclusion is a fundamental mechanism through which plants can tolerate salt concentrations (Munnes and James 2003, Garthwaite et al 2005), which was elucidated in chickpea by retention of Na+ in root and supply of K+ to shoot in Amdoun (tolerant) and Chetoui (sensitive) (Slemi et al 2001) Water Logging Stress Excess moisture and water logging predispose plants to disease attacks and insect pests that finally affect the yield and quality of grains Given the context, at flowering stage, water logging U C JHA, S K CHATURVEDI, A BOHRA et al causes mortality in chickpea ranging from 10% (line 946-512) to 65% (cv ‘Amethyst’) (Singh and Singh 2011) The mortality of plants increased with water logging just before and after flowering of plant confirming 13% mortality of plants under water logging for days before flowering The mortality rates were recorded as 65% and 100% with water logging one day after flowering and 7.5 days after flowering, respectively (Cowie et al 1995) Similarly, a set of 100 accessions was grown in excess 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