Functional & Integrative Genomics

, Volume 17, Issue 6, pp 711–723 | Cite as

Genetic dissection of plant growth habit in chickpea

  • Hari D. Upadhyaya
  • Deepak Bajaj
  • Rishi Srivastava
  • Anurag Daware
  • Udita Basu
  • Shailesh Tripathi
  • Chellapilla Bharadwaj
  • Akhilesh K. Tyagi
  • Swarup K. ParidaEmail author
Original Article


A combinatorial genomics-assisted breeding strategy encompassing association analysis, genetic mapping and expression profiling is found most promising for quantitative dissection of complex traits in crop plants. The present study employed GWAS (genome-wide association study) using 24,405 SNPs (single nucleotide polymorphisms) obtained with genotyping-by-sequencing (GBS) of 92 sequenced desi and kabuli accessions of chickpea. This identified eight significant genomic loci associated with erect (E)/semi-erect (SE) vs. spreading (S)/semi-spreading (SS)/prostrate (P) plant growth habit (PGH) trait differentiation regardless of diverse desi and kabuli genetic backgrounds of chickpea. These associated SNPs in combination explained 23.8% phenotypic variation for PGH in chickpea. Five PGH-associated genes were validated successfully in E/SE and SS/S/P PGH-bearing parental accessions and homozygous individuals of three intra- and interspecific RIL (recombinant inbred line) mapping populations as well as 12 contrasting desi and kabuli chickpea germplasm accessions by selective genotyping through Sequenom MassARRAY. The shoot apical, inflorescence and floral meristems-specific expression, including upregulation (seven-fold) of five PGH-associated genes especially in germplasm accessions and homozygous RIL mapping individuals contrasting with E/SE PGH traits was apparent. Collectively, this integrated genomic strategy delineated diverse non-synonymous SNPs from five candidate genes with strong allelic effects on PGH trait variation in chickpea. Of these, two vernalization-responsive non-synonymous SNP alleles carrying SNF2 protein-coding gene and B3 transcription factor associated with PGH traits were found to be the most promising in chickpea. The SNP allelic variants associated with E/SE/SS/S PGH trait differentiation were exclusively present in all cultivated desi and kabuli chickpea accessions while wild species/accessions belonging to primary, secondary and tertiary gene pools mostly contained prostrate PGH-associated SNP alleles. This indicates strong adaptive natural/artificial selection pressure (Tajima’s D 3.15 to 4.57) on PGH-associated target genomic loci during chickpea domestication. These vital leads thus have potential to decipher complex transcriptional regulatory gene function of PGH trait differentiation and for understanding the selective sweep-based PGH trait evolution and domestication pattern in cultivated and wild chickpea accessions adapted to diverse agroclimatic conditions. Collectively, the essential inputs generated will be of profound use in marker-assisted genetic enhancement to develop cultivars with desirable plant architecture of erect growth habit types in chickpea.


Chickpea GWAS Plant growth habit QTL SNP 



The authors gratefully acknowledge the financial support for this study provided by a research grant from the Department of Biotechnology (DBT), Government of India (102/IFD/SAN/2161/2013-14).

Supplementary material

10142_2017_566_MOESM1_ESM.pdf (298 kb)
Figure S1 (PDF 298 kb)
10142_2017_566_MOESM2_ESM.pdf (35 kb)
Table S1 (PDF 35 kb)
10142_2017_566_MOESM3_ESM.pdf (181 kb)
Table S2 (PDF 180 kb)
10142_2017_566_MOESM4_ESM.pdf (1.8 mb)
Table S3 (PDF 1880 kb)


  1. Abbo S, van-Oss Pinhasi R, Gopher A, Saranga Y, Ofner I, Peleg Z (2014) Plant domestication versus crop evolution: a conceptual framework for cereals and grain legumes. Trends Plant Sci 19:351–360CrossRefPubMedGoogle Scholar
  2. Agarwal P, Kapoor S, Tyagi AK (2011) Transcription factors regulating the progression of monocot and dicot seed development. BioEssays 33:189–202CrossRefPubMedGoogle Scholar
  3. Akpinar BA, Lucas S, Budak H (2017) A large-scale chromosome-specific SNP discovery guideline. Funct Integr Genomics 17:97–105CrossRefPubMedGoogle Scholar
  4. Aryamanesh N, Nelson MN, Yan G, Clarke HJ, Siddique KHM (2010) Mapping a major gene for growth habit and QTLs for Ascochyta blight resistance and flowering time in a population between chickpea and Cicer reticulatum. Euphytica 173:307–319CrossRefGoogle Scholar
  5. Bajaj D, Upadhyaya HD, Khan Y, Das S, Badoni S, Shree T, Kumar V, Tripathi S, Gowda CLL, Singh S, Sharma S, Tyagi AK, Chattopdhyay D, Parida SK (2015a) A combinatorial approach of comprehensive QTL-based comparative genome mapping and transcript profiling identified a seed weight-regulating candidate gene in chickpea. Sci Rep 5:9264CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bajaj D, Das S, Upadhyaya HD, Ranjan R, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015b) A genome-wide combinatorial strategy dissects complex genetic architecture of seed coat color in chickpea. Front Plant Sci 6:979CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bajaj D, Saxena MS, Kujur A, Das S, Badoni S, Tripathi S, Upadhyaya HD, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015c) Genome-wide conserved non-coding microsatellite (CNMS) marker-based integrative genetical genomics for quantitative dissection of seed weight in chickpea. J Exp Bot 66:1271–1290CrossRefPubMedGoogle Scholar
  8. Bajaj D, Upadhyaya HD, Das S, Kumar V, Gowda CLL, Sharma S, Tyagi AK, Parida SK (2016) Identification of candidate genes for dissecting complex branch number trait in chickpea. Plant Sci 245:61–70CrossRefPubMedGoogle Scholar
  9. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  10. Benlloch R, Berbel A, Ali L, Gohari G, Millán T, Madueño F (2015) Genetic control of inflorescence architecture in legumes. Front Plant Sci 6:543CrossRefPubMedPubMedCentralGoogle Scholar
  11. Borghi L, Kang J, Ko D, Lee Y, Martinoia E (2015) The role of ABCG-type ABC transporters in phytohormone transport. Biochem Soc Trans 43:924–930CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cobos MJ, Winter P, Kharrat M, Cubero JI, Gil J, Milian T, Rubio J (2009) Genetic analysis of agronomic traits in a wide cross of chickpea. Field Crops Res 111:130–136CrossRefGoogle Scholar
  13. Das S, Upadhyaya HD, Bajaj D, Kujur A, Badoni S, Laxmi, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015) Deploying QTL-seq for rapid delineation of a potential candidate gene underlying major trait-associated QTL in chickpea. DNA Res 22:193–203Google Scholar
  14. Das S, Singh M, Srivastava R, Bajaj D, Saxena MS, Rana JC, Bansal KC, Tyagi AK, Parida SK (2016) mQTL-seq delineates functionally relevant candidate gene harbouring a major QTL regulating pod number in chickpea. DNA Res 23:53–65PubMedGoogle Scholar
  15. Feuillet C, Stein N, Rossini L, Praud S, Mayer K, Schulman A, Eversole K, Appels R (2012) Integrating cereal genomics to support innovation in the Triticeae. Funct Integr Genomics 12:573–583CrossRefPubMedPubMedCentralGoogle Scholar
  16. Folta A, Bargsten JW, Bisseling T, Nap JP, Mlynarova L (2016) Compact tomato seedlings and plants upon overexpression of a tomato chromatin remodelling ATPase gene. Plant Biotechnol J 14:581–591CrossRefPubMedGoogle Scholar
  17. Gaur R, Azam S, Jeena G, Khan AW, Choudhary S, Jain M, Yadav G, Tyagi AK, Chattopadhyay D, Bhatia S (2012) High-throughput SNP discovery and genotyping for constructing a saturated linkage map of chickpea (Cicer arietinum L.) DNA Res 19:357–373CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gupta S, Nawaz K, Parween S, Roy R, Sahu K, Pole AK, Khandal H, Srivastava R, Parida SK, Chattopadhyay D (2016) Draft genome sequence of Cicer reticulatum L., the wild progenitor of chickpea provides a resource for agronomic trait improvement. DNA Res 24:1–10PubMedCentralGoogle Scholar
  19. Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, Shah N, Singh VK, Garg R, Jeena G, Yadav M, Kant C, Sharma P, Yadav G, Bhatia S, Tyagi AK, Chattopadhyay D (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.) Plant J 74:715–729CrossRefPubMedGoogle Scholar
  20. Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E (2011) Plant ABC transporters. Arabidopsis book 9:e0153CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kelly G, Sade N, Attia Z, Secchi F, Zwieniecki M, Holbrook NM, Levi A, Alchanatis V, Moshelion M, Granot D (2014) Relationship between hexokinase and the aquaporin PIP1 in the regulation of photosynthesis and plant growth. PLoS One 9:e87888CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kujur A, Bajaj D, Saxena MS, Tripathi S, Upadhyaya HD, Gowda CLL, Singh S, Jain M, Tyagi AK, Parida SK (2013) Functionally relevant microsatellite markers from chickpea transcription factor genes for efficient genotyping applications and trait association mapping. DNA Res 20:355–374CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kujur A, Bajaj D, Saxena MS, Tripathi S, Upadhyaya HD, Gowda CLL, Singh S, Tyagi AK, Jain M, Parida SK (2014) An efficient and cost-effective approach for genic microsatellite marker-based large-scale trait association mapping: identification of candidate genes for seed weight in chickpea. Mol Breed 34:241–265CrossRefGoogle Scholar
  24. Kujur A, Bajaj D, Upadhyaya HD, Das S, Ranjan R, Shree T, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015a) A genome-wide SNP scan accelerates trait-regulatory genomic loci identification in chickpea. Sci Rep 5:11166CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kujur A, Bajaj D, Upadhyaya HD, Das S, Ranjan R, Shree T, Saxena MS, Badoni S, Kumar V, Tripathi S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015b) Employing genome-wide SNP discovery and genotyping strategy to extrapolate the natural allelic diversity and domestication patterns in chickpea. Front Plant Sci 6:162CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kujur A, Upadhyaya HD, Shree T, Bajaj D, Das S, Saxena M, Badoni S, Kumar V, Tripathy S, Gowda CLL, Sharma S, Singh S, Tyagi AK, Parida SK (2015c) Ultra-high density intra-specific genetic linkage maps accelerate identification of functionally relevant molecular tags governing important agronomic traits in chickpea. Sci Rep 5:9468CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kumar A, Choudhary AK, Solanki RK, Pratap A (2011) Towards marker-assisted selection in pulses: a review. Plant breed 130:297–313CrossRefGoogle Scholar
  28. Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 2:2397–2399CrossRefGoogle Scholar
  29. Liu Z, Zhu C, Jiang Y, Tian Y, Yu J, An H, Tang W, Sun J, Tang J, Chen G, Zhai H, Wang C, Wan J (2016) Association mapping and genetic dissection of nitrogen use efficiency-related traits in rice (Oryza sativa L.) Funct Integr Genomics 16:323–333CrossRefPubMedGoogle Scholar
  30. Meyer RS, DuVal AE, Jensen HR (2012) Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytol 196:29–48CrossRefPubMedGoogle Scholar
  31. Nodzon LA, Xu WH, Wang Y, Pi LY, Chakrabarty PK, Song WY (2004) The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J 40:996–1006CrossRefPubMedGoogle Scholar
  32. Parween S, Nawaz K, Roy R, Pole AK, Venkata Suresh B, Misra G, Jain M, Yadav G, Parida SK, Tyagi AK, Bhatia S, Chattopadhyay D (2015) An advanced draft genome assembly of a desi type chickpea (Cicer arietinum L.) Sci Rep 5:12806CrossRefPubMedPubMedCentralGoogle Scholar
  33. Ryan DP, Owen-Hughes T (2011) Snf2-family proteins: chromatin remodellers for any occasion. Curr Opin Chem Biol 15:649–656CrossRefPubMedPubMedCentralGoogle Scholar
  34. Sacharowski SP, Gratkowska DM, Sarnowska EA, Kondrak P, Jancewicz I, Porri A, Bucior E, Rolicka AT, Franzen R, Kowalczyk J, Pawlikowska K, Huettel B, Torti S, Schmelzer E, Coupland G, Jerzmanowski A, Koncz C, Sarnowski TJ (2015) SWP73 subunits of Arabidopsis SWI/SNF chromatin remodeling complexes play distinct roles in leaf and flower development. Plant Cell 27:1889–1906CrossRefPubMedPubMedCentralGoogle Scholar
  35. Saxena MS, Bajaj D, Kujur A, Das S, Badoni S, Kumar V, Singh M, Bansal KC, Tyagi AK, Parida SK (2014a) Natural allelic diversity, genetic structure and linkage disequilibrium pattern in wild chickpea. PLoS One 9:e107484CrossRefPubMedPubMedCentralGoogle Scholar
  36. Saxena MS, Bajaj D, Das S, Kujur A, Kumar V, Singh M, Bansal KC, Tyagi AK, Parida SK (2014b) An integrated genomic approach for rapid delineation of candidate genes regulating agro-morphological traits in chickpea. DNA Res 21:695–710CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sharma M, Pandey GK (2016) Expansion and function of repeat domain proteins during stress and development in plants. Front Plant Sci 6:1218PubMedPubMedCentralGoogle Scholar
  38. Thudi M, Upadhyaya HD, Rathore A, Gaur PM, Krishnamurthy L, Roorkiwal M, Nayak SN, Chaturvedi SK, Basu PS, Gangarao NV, Fikre A, Kimurto P, Sharma PC, Sheshashayee MS, Tobita S, Kashiwagi J, Ito O, Killian A, Varshney RK (2014) Genetic dissection of drought and heat tolerance in chickpea through genome-wide and candidate gene-based association mapping approaches. PLoS One 9:e96758CrossRefPubMedPubMedCentralGoogle Scholar
  39. Upadhyaya HD, Furman BJ, Dwivedi SL, Udupaa SM, Gowdaa CLL, Bauma M, Croucha JH, Buhariwallaa HK, Singh S (2006) Development of a composite collection for mining germplasm possessing allelic variation for beneficial traits in chickpea. Plant Genet Resour 4:13–19CrossRefGoogle Scholar
  40. Upadhyaya HD, Dwivedi SL, Baum M, Varshney RK, Udupa SM, Gowda CLL, Hoisington D, Singh S (2008) Genetic structure, diversity and allelic richness in composite collection and reference set in chickpea (Cicer arietinum L.) BMC Plant Biol 8:106CrossRefPubMedPubMedCentralGoogle Scholar
  41. Upadhyaya HD, Bajaj D, Das S, Saxena MS, Badoni S, Kumar V, Tripathi S, Sharma S, Tyagi AK, Parida SK (2015) A genome-scale integrated approach aids in genetic dissection of complex flowering time trait in chickpea. Plant Mol Biol 89:403–420CrossRefPubMedGoogle Scholar
  42. Upadhyaya HD, Bajaj D, Narnoliya L, Das S, Kumar V, Gowda CLL, Sharma S, Tyagi AK, Parida SK (2016) Genome-wide scans for delineation of candidate genes regulating seed-protein content in chickpea. Front Plant Sci 7:302CrossRefPubMedPubMedCentralGoogle Scholar
  43. Varshney RK, Song C, Saxena RK et al. (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31:240–246Google Scholar
  44. Varshney RK, Mir RR, Bhatia S, Thudi M, Hu Y, Azam S, Zhang Y, Jaganathan D, You FM, Gao J, Riera-Lizarazu O, Luo MC (2014) Integrated physical, genetic and genome map of chickpea (Cicer arietinum L.) Funct Integr Genomics 14:59–73CrossRefPubMedPubMedCentralGoogle Scholar
  45. Wang Y, Li J, (2008) Molecular basis of plant architecture. Annu Rev Plant Biol 59(1):253–279Google Scholar
  46. Waterworth WM, Masnavi G, Bhardwaj RM, Jiang Q, Bray CM, West CE (2010) A plant DNA ligase is an important determinant of seed longevity. Plant J 63:848–860CrossRefPubMedGoogle Scholar
  47. Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L, Li J, He W, Zhang G, Zheng X, Zhang F, Li Y, Yu C, Kristiansen K, Zhang X, Wang J, Wright M, McCouch S, Nielsen R, Wang J, Wang W (2011) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105–111CrossRefPubMedGoogle Scholar
  48. Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–368CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Hari D. Upadhyaya
    • 1
  • Deepak Bajaj
    • 2
  • Rishi Srivastava
    • 2
  • Anurag Daware
    • 2
  • Udita Basu
    • 2
  • Shailesh Tripathi
    • 3
  • Chellapilla Bharadwaj
    • 3
  • Akhilesh K. Tyagi
    • 2
    • 4
  • Swarup K. Parida
    • 2
    Email author
  1. 1.International Crops Research Institute for the Semi-Arid Tropics (ICRISAT)PatancheruIndia
  2. 2.National Institute of Plant Genome Research (NIPGR)New DelhiIndia
  3. 3.Division of GeneticsIndian Agricultural Research Institute (IARI)New DelhiIndia
  4. 4.Department of Plant Molecular BiologyUniversity of Delhi South CampusNew DelhiIndia

Personalised recommendations