Drought Stress in Chickpea: Physiological, Breeding, and Omics Perspectives

  • Muhammad Waqas
  • Muhammad Tehseen Azhar
  • Iqrar Ahmad Rana
  • Anjuman Arif
  • Rana Muhammad AtifEmail author


Chickpea (Cicer arietinum L.) is a highly rich source of protein and is documented as the second most valuable food legume worldwide. In rain-fed areas, the chickpea productivity is strictly threatened by abiotic stress; notably among them is terminal drought stress. Drought stress causes reduction in photosynthesis and stomatal conductance that leads to the biosynthesis of ABA. Consequently, the plant faces oxidative stress, which is produced by ROS: H2O2, O2, O, and HO. As a result, the plant defense system is activated in the form of antioxidants (CAT, APX, POD, etc.) and scavengers (e.g., proline). In this scenario, the integration of conventional breeding with omics approaches is the ideal approach to increase the worth of the breeding program. The breeding program based on omics approaches, that is, genomics, transcriptomics, proteomics, metabolomics, ionomics, and phenomics, is the quickest and efficient way to develop drought-tolerant chickpea accessions. Moreover, the availability of high-throughput sequencing tools accelerates the working efficiency and quality of these omics approaches. Drought-responsive genes, regulatory TFs, and metabolic pathways can be identified through RNA-Seq. The worth and efficiency of the breeding program will be increased by exploiting the omics-based breeding strategies in chickpea against drought stress.


Chickpea Omics Functional genomics Drought stress Oxidative stress QTLs 



The authors acknowledge the Punjab Agricultural Research Board (Government of Punjab), Lahore, Pakistan for funding through Project PARB-938, as well as Centre for Advanced Studies in Agriculture and Food Security (CAS-AFS).


  1. Ali L, Deokar A, Caballo C, Tar’an B, Gil J, Chen W, Millan T, Rubio J (2016) Fine mapping for double podding gene in chickpea. Theor Appl Genet 129(1):77–86PubMedCrossRefGoogle Scholar
  2. Allard R (1960) Principles of plant breeding, vol 36. John Willey and Sons, Inc, New York, NYGoogle Scholar
  3. Almeselmani M, Deshmukh P, Sairam R, Kushwaha S, Singh T (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171(3):382–388PubMedCrossRefGoogle Scholar
  4. Armand N, Amiri H, Ismaili A (2016) Interaction of methanol spray and water‐deficit stress on photosynthesis and biochemical characteristics of Phaseolus vulgaris L. cv. Sadry. Photochem Photobiol 92(1):102–110PubMedCrossRefGoogle Scholar
  5. Badhan S, Kole P, Ball A, Mantri N (2018) RNA sequencing of leaf tissues from two contrasting chickpea genotypes reveals mechanisms for drought tolerance. Plant Physiol Biochem 129:295–304PubMedCrossRefGoogle Scholar
  6. Baginsky S, Hennig L, Zimmermann P, Gruissem W (2010) Gene expression analysis, proteomics, and network discovery. Plant Physiol 152(2):402–410PubMedPubMedCentralCrossRefGoogle Scholar
  7. Basu P, Ali M, Chaturvedi S (2007a) Osmotic adjustment increases water uptake, remobilization of assimilates and maintains photosynthesis in chickpea under drought. Indian J Exp Biol 45(3):261–267PubMedGoogle Scholar
  8. Basu P, Berger J, Turner N, Chaturvedi S, Ali M, Siddique K (2007b) Osmotic adjustment of chickpea (Cicer arietinum) is not associated with changes in carbohydrate composition or leaf gas exchange under drought. Ann Appl Biol 150(2):217–225CrossRefGoogle Scholar
  9. Bhushan D, Pandey A, Choudhary MK, Datta A, Chakraborty S, Chakraborty N (2007) Comparative proteomics analysis of differentially expressed proteins in chickpea extracellular matrix during dehydration stress. Mol Cell Proteomics 6(11):1868–1884PubMedCrossRefGoogle Scholar
  10. Buchanan CD, Lim S, Salzman RA, Kagiampakis I, Morishige DT, Weers BD, Klein RR, Pratt LH, Cordonnier-Pratt M-M, Klein PE (2005) Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol Biol 58(5):699–720PubMedCrossRefGoogle Scholar
  11. Çevik S, Akpinar G, Yildizli A, Kasap M, Karaosmanoğlu K, Ünyayar S (2019) Comparative physiological and leaf proteome analysis between drought-tolerant chickpea Cicer reticulatum and drought-sensitive chickpea C. arietinum. J Biosci (Bangalore) 44(1):20Google Scholar
  12. Chandra S, Buhariwalla H, Kashiwagi J, Harikrishna S (2004) Identifying QTL-linked markers in marker-deficient crops. Markers 2(38.1):235Google Scholar
  13. Chattopadhyay A, Chakraborty S, Bhushan D, Chakraborty N, Datta A, Choudhary MK, Pandey A (2006) Extracellular matrix proteome of chickpea (Cicer arietinum) illustrates pathway abundance, novel protein functions and evolutionary perspect. Am Chem Soc 5(7):1711–1720Google Scholar
  14. Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field? Photosynthesis and growth. Ann Bot 89(7):907–916PubMedPubMedCentralCrossRefGoogle Scholar
  15. Collard BC, Mackill DJ (2007) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Phil Trans R Soc B Biol Sci 363(1491):557–572CrossRefGoogle Scholar
  16. Crossa J, Perez P, Hickey J, Burgueño J, Ornella L, Cerón-Rojas J, Zhang X, Dreisigacker S, Babu R, Li Y (2014) Genomic prediction in CIMMYT maize and wheat breeding programs. Heredity 112(1):48PubMedCrossRefGoogle Scholar
  17. Dalvi U, Naik R, Lokhande P (2018) Antioxidant defense system in chickpea against drought stress at pre-and post-flowering stages. Indian J Plant Physiol 23(1):16–23CrossRefGoogle Scholar
  18. Das A, Eldakak M, Paudel B, Kim D-W, Hemmati H, Basu C, Rohila JS (2016) Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean. Bio Med Res Int 2016:6021047Google Scholar
  19. Deokar AA, Kondawar V, Jain PK, Karuppayil SM, Raju N, Vadez V, Varshney RK, Srinivasan R (2011) Comparative analysis of expressed sequence tags (ESTs) between drought-tolerant and-susceptible genotypes of chickpea under terminal drought stress. BMC Plant Biol 11(1):70PubMedPubMedCentralCrossRefGoogle Scholar
  20. Eldakak M, Milad SI, Nawar AI, Rohila JS (2013) Proteomics: a biotechnology tool for crop improvement. Front Plant Sci 4:35PubMedPubMedCentralCrossRefGoogle Scholar
  21. Fang X, Turner NC, Yan G, Li F, Siddique KH (2009) Flower numbers, pod production, pollen viability, and pistil function are reduced and flower and pod abortion increased in chickpea (Cicer arietinum L.) under terminal drought. J Exp Bot 61(2):335–345PubMedPubMedCentralCrossRefGoogle Scholar
  22. Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi S, Siddique K (2017) Drought stress in grain legumes during reproduction and grain filling. J Agric Crop Sci 203(2):81–102CrossRefGoogle Scholar
  23. Flowers TJ, Gaur PM, Gowda CL, Krishnamurthy L, Samineni S, Siddique KH, Turner NC, Vadez V, Varshney RK, Colmer TD (2010) Salt sensitivity in chickpea. Plant Cell Environ 33(4):490–509PubMedCrossRefGoogle Scholar
  24. Gao W-R, Wang X-S, Liu Q-Y, Peng H, Chen C, Li J-G, Zhang J-S, Hu S-N, Ma H (2008) Comparative analysis of ESTs in response to drought stress in chickpea (C. arietinum L.). Biochem Biophys Res Commun 376(3):578–583PubMedCrossRefGoogle Scholar
  25. Garg R, Patel RK, Jhanwar S, Priya P, Bhattacharjee A, Yadav G, Bhatia S, Chattopadhyay D, Tyagi AK, Jain M (2011) Gene discovery and tissue-specific transcriptome analysis in chickpea with massively parallel pyrosequencing and web resource development. Plant Physiol 156(4):1661–1678PubMedPubMedCentralCrossRefGoogle Scholar
  26. Garg R, Bhattacharjee A, Jain M (2015) Genome-scale transcriptomic insights into molecular aspects of abiotic stress responses in chickpea. Plant Mol Biol Rep 33(3):388–400CrossRefGoogle Scholar
  27. Garg R, Shankar R, Thakkar B, Kudapa H, Krishnamurthy L, Mantri N, Varshney RK, Bhatia S, Jain M (2016) Transcriptome analyses reveal genotype-and developmental stage-specific molecular responses to drought and salinity stresses in chickpea. Sci Rep 6:19228PubMedPubMedCentralCrossRefGoogle Scholar
  28. Gayen D, Gayali S, Barua P, Lande NV, Varshney S, Sengupta S, Chakraborty S, Chakraborty N (2019) Dehydration-induced proteomic landscape of mitochondria in chickpea reveals large-scale coordination of key biological processes. J Proteomics 192:267–279PubMedCrossRefGoogle Scholar
  29. Govt. of Pakistan (2016–2017) Economic survey of Pakistan. Ministry of Finance, Economic Advisors’s Wing, IslamabadGoogle Scholar
  30. Gupta P, Rustgi S (2004) Molecular markers from the transcribed/expressed region of the genome in higher plants. Funct Integr Genomics 4(3):139–162PubMedCrossRefGoogle Scholar
  31. Gupta S, Rathore A, Sharma S, Saini R (2000) Response of chickpea cultivars to water stress. Indian J Plant Physiol 5(3):274–276Google Scholar
  32. Gupta S, Nawaz K, Parween S, Roy R, Sahu K, Kumar Pole A, Khandal H, Srivastava R, Kumar Parida S, Chattopadhyay D (2016) Draft genome sequence of Cicer reticulatum L., the wild progenitor of chickpea provides a resource for agronomic trait improvement. DNA Res 24(1):1–10Google Scholar
  33. Haake V, Cook D, Riechmann J, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130(2):639–648PubMedPubMedCentralCrossRefGoogle Scholar
  34. Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156(1-2):1–13CrossRefGoogle Scholar
  35. Hamanishi ET, Thomas BR, Campbell MM (2012) Drought induces alterations in the stomatal development program in Populus. J Exp Bot 63(13):4959–4971PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hamwieh A, Imtiaz M, Malhotra R (2013) Multi-environment QTL analyses for drought-related traits in a recombinant inbred population of chickpea (Cicer arientinum L.). Theor Appl Genet 126(4):1025–1038PubMedCrossRefGoogle Scholar
  37. Haq M (2009) Development of mutant varieties of crop plants at NIAB and the impact on agricultural production in Pakistan. Induced plant mutations in the genomics era. Food and Agriculture Organization of the United Nations, Rome, pp 61–64Google Scholar
  38. Harris D, Tripathi R, Joshi A (2002) On-farm seed priming to improve crop establishment and yield in dry direct-seeded rice. Direct seeding: research strategies and opportunities. International Research Institute, Manila, pp 231–240Google Scholar
  39. Hawkes J (1977) The importance of wild germplasm in plant breeding. Euphytica 26(3):615–621CrossRefGoogle Scholar
  40. Hayes B, Goddard M (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157(4):1819–1829PubMedPubMedCentralGoogle Scholar
  41. Hayes BJ, Bowman PJ, Chamberlain A, Goddard M (2009) Invited review: genomic selection in dairy cattle: progress and challenges. J Dairy Sci 92(2):433–443PubMedCrossRefGoogle Scholar
  42. Hufford MB, Lubinksy P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J (2013) The genomic signature of crop-wild introgression in maize. PLoS Genet 9(5):e1003477PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hussain A, Tanveer R, Mustafa G, Farooq M, Amin I, Mansoor S (2019) Comparative phylogenetic analysis of aquaporins provides insight into the gene family expansion and evolution in plants and their role in drought tolerant and susceptible chickpea cultivars. Genomics.
  44. Jaganathan D, Thudi M, Kale S, Azam S, Roorkiwal M, Gaur PM, Kishor PK, Nguyen H, Sutton T, Varshney RK (2015) Genotyping-by-sequencing based intra-specific genetic map refines a “QTL-hotspot” region for drought tolerance in chickpea. Mol Genet Genomics 290(2):559–571PubMedCrossRefGoogle Scholar
  45. Jain D, Chattopadhyay D (2010) Analysis of gene expression in response to water deficit of chickpea (Cicer arietinum L.) varieties differing in drought tolerance. BMC Plant Biol 10(1):24PubMedPubMedCentralCrossRefGoogle Scholar
  46. Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, Shah N, Singh VK, Garg R, Jeena G (2013) A draft genome sequence of the pulse crop chickpea (C icer arietinum L.). Plant J 74(5):715–729PubMedCrossRefGoogle Scholar
  47. Jamalabadi JG, Saidi A, Karami E, Kharkesh M, Talebi R (2013) Molecular mapping and characterization of genes governing time to flowering, seed weight, and plant height in an intraspecific genetic linkage map of chickpea (Cicer arietinum). Biochem Genet 51(5-6):387–397PubMedCrossRefGoogle Scholar
  48. Jha UC (2018) Current advances in chickpea genomics: applications and future perspectives. Plant Cell Rep 37:947–965PubMedCrossRefGoogle Scholar
  49. Joseph B, Jini D, Sujatha S (2011) Development of salt stress-tolerant plants by gene manipulation of antioxidant enzymes. Asian J Agric Res 5(1):17–27Google Scholar
  50. Jukanti A, Gaur P, Gowda C, Chibbar R (2012) Chickpea: nutritional properties and its benefits. Br J Nutr 108:S11–S26PubMedCrossRefGoogle Scholar
  51. Kahraman A, Pandey A, Khan MK, Lindsay D, Moenga S, Vance L, Bergmann E, Carrasquilla-Garcia N, Shin M-G, Chang PL (2017) Distinct subgroups of Cicer echinospermum are associated with hybrid sterility and breakdown in interspecific crosses with cultivated Chickpea. Crop Sci 57(6):3101–3111Google Scholar
  52. Kale SM, Jaganathan D, Ruperao P, Chen C, Punna R, Kudapa H, Thudi M, Roorkiwal M, Katta MA, Doddamani D (2015) Prioritization of candidate genes in “QTL-hotspot” region for drought tolerance in chickpea (Cicer arietinum L.). Sci Rep 5:15296PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kalefetoğlu Macar T, Ekmekçi Y (2009) Alterations in photochemical and physiological activities of chickpea (Cicer arietinum L.) cultivars under drought stress. J Agric Crop Sci 195(5):335–346CrossRefGoogle Scholar
  54. Kalra N, Chakraborty D, Sharma A, Rai H, Jolly M, Chander S, Kumar PR, Bhadraray S, Barman D, Mittal R (2008) Effect of increasing temperature on yield of some winter crops in northwest India. Curr Sci 94:82–88Google Scholar
  55. Kashiwagi J, Krishnamurthy L, Upadhyaya HD, Krishna H, Chandra S, Vadez V, Serraj R (2005) Genetic variability of drought-avoidance root traits in the mini-core germplasm collection of chickpea (Cicer arietinum L.). Euphytica 146(3):213–222CrossRefGoogle Scholar
  56. Kaur K, Kaur N, Gupta AK, Singh I (2013) Exploration of the antioxidative defense system to characterize chickpea genotypes showing differential response towards water deficit conditions. Plant Growth Regul 70(1):49–60CrossRefGoogle Scholar
  57. Khan H, Gul R, Khan N, Naz R, Shah S, Asim N, Latif A (2018) Role of selection indices in ascertaining high yielding drought stress tolerant chickpea (Cicer arietinum L.). J Anim Plant Sci 28(1):146Google Scholar
  58. Komatsu S, Mock H-P, Yang P, Svensson B (2013) Application of proteomics for improving crop protection/artificial regulation. Front Plant Sci 4:522PubMedPubMedCentralGoogle Scholar
  59. Kudapa H, Garg V, Chitikineni A, Varshney RK (2018) The RNA‐Seq‐based high resolution gene expression atlas of chickpea (Cicer arietinum L.) reveals dynamic spatio‐temporal changes associated with growth and development. Plant Cell Environ 41(9):2209–2225PubMedGoogle Scholar
  60. Kumar J, Abbo S (2001) Genetics of flowering time in chickpea and its bearing on productivity in semiarid environments. Adv Agron 72:107–178CrossRefGoogle Scholar
  61. Lestari EG (2016) Combination of somaclonal variation and mutagenesis for crop improvement. J Agro Biogen 8(1):38–44Google Scholar
  62. Li Y, Ruperao P, Batley J, Edwards D, Khan T, Colmer TD, Pang J, Siddique KH, Sutton T (2018) Investigating drought tolerance in chickpea using genome-wide association mapping and genomic selection based on whole-genome resequencing data. Front Plant Sci 9:190PubMedPubMedCentralCrossRefGoogle Scholar
  63. Luo L, Xia H, Lu B (2019) Crop breeding for drought resistance. Front Plant Sci 10:314PubMedPubMedCentralCrossRefGoogle Scholar
  64. Mafakheri A, Siosemardeh A, Bahramnejad B, Struik P, Sohrabi Y (2010) Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Aust J Crop Sci 4(8):580Google Scholar
  65. Maluszynski M (2001) Officially released mutant varieties - the FAO/IAEA database, vol 65. IAEA, Vienna. Scholar
  66. Mashaki KM, Garg V, Ghomi AAN, Kudapa H, Chitikineni A, Nezhad KZ, Yamchi A, Soltanloo H, Varshney RK, Thudi M (2018) RNA-Seq analysis revealed genes associated with drought stress response in kabuli chickpea (Cicer arietinum L.). PLoS One 13(6):e0199774CrossRefGoogle Scholar
  67. Mir RR, Zaman-Allah M, Sreenivasulu N, Trethowan R, Varshney RK (2012) Integrated genomics, physiology and breeding approaches for improving drought tolerance in crops. Theor Appl Genet 125(4):625–645PubMedPubMedCentralCrossRefGoogle Scholar
  68. Mitchell-Olds T (2010) Complex-trait analysis in plants. Genome Biol 11(4):113PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mohammadi A, Habibi D, Rohami M, Mafakheri S (2011) Effect of drought stress on antioxidant enzymes activity of some chickpea cultivars. Am Eur J Agric Env Sci 11(6):782–785Google Scholar
  70. Mohler V, Singrün C (2004) General considerations: marker-assisted selection. Molecular marker systems in plant breeding and crop improvement. Springer, New York, NY, pp 305–317Google Scholar
  71. Molina C, Rotter B, Horres R, Udupa SM, Besser B, Bellarmino L, Baum M, Matsumura H, Terauchi R, Kahl G (2008) SuperSAGE: the drought stress-responsive transcriptome of chickpea roots. BMC Genomics 9(1):553PubMedPubMedCentralCrossRefGoogle Scholar
  72. Mozafari J, Pouresmael M, Najafi F, Khavari-Nejad R, Moradi F (2018) Identification of possible mechanisms of chickpea (Cicer arietinum L.) drought tolerance using cDNA-AFLP. J Agric Sci Technol 7:1303–1317Google Scholar
  73. Muruiki R, Kimurto P, Vandez V, Gangarao R, Silim S, Siambi M (2018) Effect of drought stress on yield performance of parental chickpea genotypes in semi-arid tropics. J Life Sci 12(3):159–168Google Scholar
  74. Omae H, Kumar A, Egawa Y, Kashiwaba K, Shono M (2005) Midday drop of leaf water content related to drought tolerance in snap bean (Phaseolus vulgaris L.). Plant Prod Sci 8(4):465–467CrossRefGoogle Scholar
  75. Pagter M, Bragato C, Brix H (2005) Tolerance and physiological responses of Phragmites australis to water deficit. Aquat Bot 81(4):285–299CrossRefGoogle Scholar
  76. Pang J, Turner NC, Khan T, Du Y-L, Xiong J-L, Colmer TD, Devilla R, Stefanova K, Siddique KH (2016) Response of chickpea (Cicer arietinum L.) to terminal drought: leaf stomatal conductance, pod abscisic acid concentration, and seed set. J Exp Bot 68(8):1973–1985PubMedCentralPubMedGoogle Scholar
  77. Parween S, Nawaz K, Roy R, Pole AK, Suresh BV, Misra G, Jain M, Yadav G, Parida SK, Tyagi AK (2015) An advanced draft genome assembly of a desi type chickpea (Cicer arietinum L.). Sci Rep 5:12806PubMedPubMedCentralCrossRefGoogle Scholar
  78. Patel PK, Hemantaranjan A (2013) Differential sensitivity of chickpea genotypes to salicylic acid and drought stress during preanthesis: effects on total chlorophyll, phenolics, seed protein and protein profiling. Bioscan 8(2):569–574Google Scholar
  79. Patwardhan A, Semenov S, Schnieder S, Burton I, Magadza C, Oppenheimer M, Pittock B, Rahman A, Smith J, Suarez A (2007) Assessing key vulnerabilities and the risk from climate change. In: Climate change. Cambridge University Press, Cambridge, pp 779–810Google Scholar
  80. Pouresmael M, Khavari-Nejad RA, Mozafari J, Najafi F, Moradi F (2013) Efficiency of screening criteria for drought tolerance in chickpea. Arch Agric Soil Sci 59(12):1675–1693CrossRefGoogle Scholar
  81. Rahbarian R, Khavari-Nejad R, Ganjeali A, Bagheri A, Najafi F (2011) Drought stress effects on photosynthesis, chlorophyll fluorescence and water relations in tolerant and susceptible chickpea (Cicer arietinum L.) genotypes. Acta Biol Cracov Bot 53(1):47–56Google Scholar
  82. Rahimizadeh M, Habibi D, Madani H, Mohammadi GN, Mehraban A, Sabet AM (2007) The effect of micronutrients on antioxidant enzymes metabolism in sunflower (helianthus annuus l.) under drought stress. Helia 30(47):167–174CrossRefGoogle Scholar
  83. Ramamoorthy P, Lakshmanan K, Upadhyaya HD, Vadez V, Varshney RK (2017) Root traits confer grain yield advantages under terminal drought in chickpea (Cicer arietinum L.). Field Crop Res 201:146–161CrossRefGoogle Scholar
  84. Rehman A, Malhotra R, Bett K, Tar’an B, Bueckert R, Warkentin T (2011) Mapping QTL associated with traits affecting grain yield in chickpea (Cicer arietinum L.) under terminal drought stress. Crop Sci 51(2):450–463CrossRefGoogle Scholar
  85. Rokhzadi A (2014) Response of chickpea (Cicer arietinum L.) to exogenous salicylic acid and ascorbic acid under vegetative and reproductive drought stress conditions. J App Bot Food Qual 87:80Google Scholar
  86. Sachdeva S, Bharadwaj C, Sharma V, Patil B, Soren K, Roorkiwal M, Varshney R, Bhat K (2018) Molecular and phenotypic diversity among chickpea (Cicer arietinum) genotypes as a function of drought tolerance. Crop Pasture Sci 69(2):142–153CrossRefGoogle Scholar
  87. Sadras VO, Lake L, Li Y, Farquharson EA, Sutton T (2016) Phenotypic plasticity and its genetic regulation for yield, nitrogen fixation and δ13C in chickpea crops under varying water regimes. J Exp Bot 67(14):4339–4351PubMedCrossRefGoogle Scholar
  88. Salimath P, Toker C, Sandhu J, Kumar J, Suma B, Yadav S, Bahl P (2007) Conventional breeding methods. Chickpea Breeding Management. CAB International, Wallingford, pp 369–390CrossRefGoogle Scholar
  89. Samineni S, Varshney RK, Sajja S, Thudi M, Jayalakshmi V, Vijayakumar A, Mannur D (2015) High yielding and drought tolerant genotypes developed through marker-assisted back crossing (MBAC) in chickpeaGoogle Scholar
  90. Samineni S, Thudi M, Sajja SB, Varshney RK, Gaur PM (2017) Impact of Genomics on Chickpea Breeding. In: The Chickpea Genome. Springer, pp 125–134Google Scholar
  91. Santisree P, Bhatnagar-Mathur P, Sharma K (2017) The leaf proteome signatures provide molecular insights into the abiotic stress tolerance in chickpea: a priming and proteomics approachGoogle Scholar
  92. Shan F, Clarke H, Plummer J, Yan G, Siddique K (2005) Geographical patterns of genetic variation in the world collections of wild annual Cicer characterized by amplified fragment length polymorphisms. Theor Appl Genet 110(2):381–391PubMedCrossRefGoogle Scholar
  93. Sharma S, Yadav N, Singh A, Kumar R (2013) Nutritional and antinutritional profile of newly developed chickpea (Cicer arietinum L) varieties. Int Food Res J 20(2):805Google Scholar
  94. Sheoran S, Singh R, Tripathi S (2018) Marker assisted backcross breeding in chickpea (Cicer arietinum L.) for drought tolerance. Int J Chem Std 6(1):1046–1050Google Scholar
  95. Silim S, Saxena M (1993) Adaptation of spring-sown chickpea to the Mediterranean basin. II. Factors influencing yield under drought. Field Crop Res 34(2):137–146CrossRefGoogle Scholar
  96. Singh B, Bohra A, Mishra S, Joshi R, Pandey S (2015) Embracing new-generation ‘omics’ tools to improve drought tolerance in cereal and food-legume crops. Biol Plant 59(3):413–428CrossRefGoogle Scholar
  97. Sinha R, Gupta A, Senthil-Kumar M (2017) Concurrent drought stress and vascular pathogen infection induce common and distinct transcriptomic responses in chickpea. Front Plant Sci 8:333PubMedPubMedCentralCrossRefGoogle Scholar
  98. Sivasakthi K, Thudi M, Tharanya M, Kale SM, Kholová J, Halime MH, Jaganathan D, Baddam R, Thirunalasundari T, Gaur PM (2018) Plant vigour QTLs co-map with an earlier reported QTL hotspot for drought tolerance while water saving QTLs map in other regions of the chickpea genome. BMC Plant Biol 18(1):29PubMedPubMedCentralCrossRefGoogle Scholar
  99. Srinivasan S (2017) High yielding and drought tolerant genotypes developed through marker-assisted back crossing (MBAC) in chickpea. In: Int Plant Breeding Cong (IPBC)-EucarpiaGoogle Scholar
  100. Sudupak M, Akkaya M, Kence A (2002) Analysis of genetic relationships among perennial and annual Cicer species growing in Turkey using RAPD markers. Theor Appl Genet 105(8):1220–1228PubMedCrossRefGoogle Scholar
  101. Summy S, Boora K, Sharma K (2016) Physiological traits in relation to yield improvement in chickpea (Cicer arietinum L.) under depleting soil moisture environment. Ind J Genet Plant Breed 76(2):209CrossRefGoogle Scholar
  102. Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Asociates. Inc, Sunderland, MAGoogle Scholar
  103. Tas S, Tas B (2007) Some physiological responses of drought stress in wheat genotypes with different ploidity in Turkiye. World J Agric Sci 3(2):178–183Google Scholar
  104. Thudi M, Gaur PM, Krishnamurthy L, Mir RR, Kudapa H, Fikre A, Kimurto P, Tripathi S, Soren KR, Mulwa R (2014a) Genomics-assisted breeding for drought tolerance in chickpea. Funct Plant Biol 41(11):1178–1190CrossRefGoogle Scholar
  105. Thudi M, Upadhyaya HD, Rathore A, Gaur PM, Krishnamurthy L, Roorkiwal M, Nayak SN, Chaturvedi SK, Basu PS, Gangarao N (2014b) Genetic dissection of drought and heat tolerance in chickpea through genome-wide and candidate gene-based association mapping approaches. PLoS One 9(5):e96758PubMedPubMedCentralCrossRefGoogle Scholar
  106. Toker C (2009) A note on the evolution of kabuli chickpeas as shown by induced mutations in Cicer reticulatum Ladizinsky. Genet Resour Crop Evol 56(1):7–12CrossRefGoogle Scholar
  107. Toker C, Canci H, Yildirim T (2007) Evaluation of perennial wild Cicer species for drought resistance. Genet Resour Crop Evol 54(8):1781–1786CrossRefGoogle Scholar
  108. Upadhyaya HD, Kashiwagi J, Varshney RK, Gaur P, Saxena K, Krishnamurthy L, Gowda C, Pundir R, Chaturvedi S, Basu P (2012) Phenotyping chickpeas and pigeonpeas for adaptation to drought. Front Physiol 3:179PubMedPubMedCentralCrossRefGoogle Scholar
  109. Varshney RK, Hiremath PJ, Lekha P, Kashiwagi J, Balaji J, Deokar AA, Vadez V, Xiao Y, Srinivasan R, Gaur PM (2009) A comprehensive resource of drought-and salinity-responsive ESTs for gene discovery and marker development in chickpea (Cicer arietinum L.). BMC Genomics 10(1):523PubMedPubMedCentralCrossRefGoogle Scholar
  110. Varshney RK, Gaur PM, Chamarthi SK, Krishnamurthy L, Tripathi S, Kashiwagi J, Samineni S, Singh VK, Thudi M, Jaganathan D (2013a) Fast-track introgression of “QTL-hotspot” for root traits and other drought tolerance traits in JG 11, an elite and leading variety of chickpea. Plant Genome 6(3):1Google Scholar
  111. Varshney RK, Mohan SM, Gaur PM, Gangarao N, Pandey MK, Bohra A, Sawargaonkar SL, Chitikineni A, Kimurto PK, Janila P (2013b) Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnol Adv 31(8):1120–1134PubMedCrossRefGoogle Scholar
  112. Varshney RK, Mir RR, Bhatia S, Thudi M, Hu Y, Azam S, Zhang Y, Jaganathan D, You FM, Gao J (2014a) Integrated physical, genetic and genome map of chickpea (Cicer arietinum L.). Funct Integr Genomics 14(1):59–73PubMedPubMedCentralCrossRefGoogle Scholar
  113. Varshney RK, Thudi M, Nayak SN, Gaur PM, Kashiwagi J, Krishnamurthy L, Jaganathan D, Koppolu J, Bohra A, Tripathi S (2014b) Genetic dissection of drought tolerance in chickpea (Cicer arietinum L.). Theor Appl Genet 127(2):445–462PubMedCrossRefGoogle Scholar
  114. Varshney RK, Thudi M, Muehlbauer FJ (2017) The chickpea genome: an introduction. In: The chickpea genome. Springer, New York, NY, pp 1–4CrossRefGoogle Scholar
  115. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57PubMedPubMedCentralCrossRefGoogle Scholar
  116. Wang X, Liu Y, Jia Y, Gu H, Ma H, Yu T, Zhang H, Chen Q, Ma L, Gu A (2012) Transcriptional responses to drought stress in root and leaf of chickpea seedling. Mol Biol Rep 39(8):8147–8158PubMedCrossRefGoogle Scholar
  117. Westbrook JA, Wheeler JX, Wait R, Welson SY, Dunn MJ (2006) The human heart proteome: two‐dimensional maps using narrow‐range immobilised pH gradients. Electrophoresis 27(8):1547–1555PubMedCrossRefGoogle Scholar
  118. William P (1987) The chickpea-nutritional quality and the evaluation of quality in breeding programmes. In: Saxena MC, Singh KB (eds) The chickpea. CAB International, WallingfordGoogle Scholar
  119. Zaman-Allah M, Jenkinson DM, Vadez V (2011a) Chickpea genotypes contrasting for seed yield under terminal drought stress in the field differ for traits related to the control of water use. Funct Plant Biol 38(4):270–281CrossRefGoogle Scholar
  120. Zaman-Allah M, Jenkinson DM, Vadez V (2011b) A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea. J Exp Bot 62(12):4239–4252PubMedPubMedCentralCrossRefGoogle Scholar
  121. Zhao S, Fung-Leung W-P, Bittner A, Ngo K, Liu X (2014) Comparison of RNA-Seq and microarray in transcriptome profiling of activated T cells. PLoS One 9(1):e78644PubMedPubMedCentralCrossRefGoogle Scholar
  122. Zhu J-K (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124(3):941–948Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Muhammad Waqas
    • 1
  • Muhammad Tehseen Azhar
    • 1
  • Iqrar Ahmad Rana
    • 2
  • Anjuman Arif
    • 3
  • Rana Muhammad Atif
    • 1
    • 2
    • 4
    Email author
  1. 1.Department of Plant Breeding and GeneticsUniversity of AgricultureFaisalabadPakistan
  2. 2.Centre of Agricultural Biochemistry and BiotechnologyUniversity of AgricultureFaisalabadPakistan
  3. 3.Plant Breeding and Genetics DivisionNuclear Institute of Agriculture and BiologyFaisalabadPakistan
  4. 4.Center for Advanced Studies in Agriculture and Food SecurityUniversity of AgricultureFaisalabadPakistan

Personalised recommendations