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Genotyping-by-sequencing and multilocation evaluation of two interspecific backcross populations identify QTLs for yield-related traits in pigeonpea

Abstract

This study has identified single-nucleotide polymorphism (SNP) markers associated with nine yield-related traits in pigeonpea by using two backcross populations (BP) developed through interspecific crosses and evaluating them at two locations and 3 years. In both the populations, markers have shown strong segregation distortion; therefore, a quantitative trait locus (QTL) mapping mixed model was used. A total of 86 QTLs explaining 12–21% phenotypic variation were detected in BP-1. On the other hand, 107 QTLs explaining 11–29% phenotypic variation were detected in BP-2. Although most QTLs were environment and trait specific, few stable and consistent QTLs were also detected. Interestingly, 11 QTLs in BP-2 were associated with more than one trait. Among these QTLs, eight QTLs associated with days to 50% flowering and days to 75% maturity were located on CcLG07. One SNP “S7_14185076” marker in BP-2 population has been found associated with four traits, namely days to 50% flowering, days to 75% maturity, primary branches per plant and secondary branches per plant with positive additive effect. Hence, the present study has not only identified QTLs for yield-related traits, but also discovered novel alleles from wild species, which can be used for improvement of traits through genomics-assisted breeding.

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References

  1. Aruna R, Manohar RD, Reddy LJ, Upadhyaya HD, Sharma HC (2005) Inheritance of trichomes and resistance to pod borer (Helicoverpa armigera) and their association in interspecific crosses between cultivated pigeonpea (Cajanus cajan) and its wild relative C. scarabaeoides. Euphytica 145:247–257

  2. Bermudez L, Urias U, Milstein D, Kamenetzky L, Asis R, Fernie AR, Van Sluys MA, Carrari F, Rossi M (2008) A candidate gene survey of quantitative trait loci affecting chemical composition in tomato fruit. J Exp Bot 59:2875–2890

  3. Bohra A, Mallikarjuna N, Saxena KB, Upadhyaya HD, Vales I, Varshney RK (2010) Harnessing the potential of crop wild relatives through genomics tools for pigeonpea improvement. J Plant Biol 37:1–16

  4. Bohra A, Dubey A, Saxena RK, Penmetsa RV, Poornima KN, Kumar N, Farmer AD, Srivani G, Upadhyaya HD, Gothalwal R, Ramesh R, Singh D, Saxena KB, Kavikishor PB, Town CD, May GD, Cook DR, Varshney RK (2011) Analysis of BAC-end sequences (BESs) and development of BES-SSR markers for genetic mapping and hybrid purity assessment in pigeonpea (Cajanus spp.). BMC Plant Biol 11:56

  5. Bohra A, Saxena RK, Gnanesh BN, Saxena KB, Byregowda M, Rathore A, Kavi Kishor PB, Cook DR, Varshney RK (2012) An intra-specific consensus genetic map of pigeonpea (Cajanus cajan (L.) Millsp.) derived from six mapping populations. Theor Appl Genet 125:1325–1338

  6. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

  7. Chen J, Li X, Cheng C, Wang Y, Qin M, Zhu H, Zeng R, Fu X, Liu Z, Zhang G (2014) Characterization of epistatic interaction of QTLs LH8 and EH3 controlling heading date in rice. Sci Rep 4:4263

  8. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379

  9. Gnanesh BN, Bohra A, Sharma M, Byregowda M, Pande S, Wesley V, Saxena RK, Saxena KB, Kavi Kishor PB, Varshney RK (2011) Genetic mapping and quantitative trait locus analysis of resistance to sterility mosaic disease in pigeonpea [Cajanus cajan (L.) Millsp.]. Field Crop Res 123:53–61

  10. Gyenis L, Yun SJ, Smith KP, Steffenson BJ, Bossolini E, Muehlbauer GJ (2007) Genetic architecture of quantitative trait loci associated with morphological and agronomic trait differences in a wild by cultivated barley cross. Genome 50:714–723

  11. ICRISAT (1993) Pigeonpea variety ICPL 87119. Plant material description no.43. Documentation. International Crops Research Institute for the Semi-Arid Tropics. https://oar.icrisat.org/566/1/PMD_43.pdf. Accessed 5 Apr 2019

  12. Jadhav DR, Mallikarjuna N, Sharma HC, Saxena KB (2012) Introgression of Helicoverpa armigera resistance from Cajanus acutifolius—a wild relative from secondary gene pool of pigeonpea (Cajanus cajan). Asian J Agric Sci 4:242–248

  13. Khera P, Pandey MK, Mallikarjuna N, Sriswathi M, Roorkiwal M, Janila P, Sharma S, Shilpa K, Sudini H, Guo B, Varshney RK (2019) Genetic imprints of domestication for disease resistance, oil quality, and yield component traits in groundnut (Arachis hypogaea L.). Mol Genet Genom 294:365–378

  14. Kumar V, Khan AW, Saxena RK, Garg V, Varshney RK (2016) First-generation HapMap in Cajanus spp. reveals untapped variations in parental lines of mapping populations. Plant Biotechnol J. 14:1673–1681

  15. Li P, Kirungu JN, Lu H, Magwanga RO, Lu P, Cai X, Zhou Z, Wang X, Hou Y, Wang Y, Xu Y (2018) SSR-Linkage map of interspecific populations derived from Gossypium trilobum and Gossypium thurberi and determination of genes harbored within the segregating distortion regions. PLoS ONE 13:e0207271

  16. Lorieux M (2005) CSSL finder: a free program for managing introgression lines. https://mapdisto.free.fr/CSSLFinder/. Accessed 20 Aug 2018

  17. Malosetti M, van Eeuwijk FA, Boer MP, Casas AM, Elía M, Moralejo M, Bhat PR, Ramsay L, Molina-Cano JL (2011) Gene and QTL detection in a three-way barley cross under selection by a mixed model with kinship information using SNPs. Theor Appl Genet 122:1605–1616

  18. Manrique-Carpintero NC, Coombs JJ, Veilleux RE, Buell CR, Douches DS (2016) Comparative analysis of regions with distorted segregation in three diploid populations of potato. G3 Gen Genom Genet 6:2617–2628

  19. Mora F, Quitral YA, Matus I, Russell J, Waugh R, del Pozo A (2016) SNP-based QTL mapping of 15 complex traits in barley under rain-fed and well-watered conditions by a mixed modeling approach. Front Plant Sci 7:909

  20. Obala J, Saxena RK, Singh V, Sameer Kumar CV, Saxena KB, Tongoona P, Sibiya J, Varshney RK (2019) Development of sequence-based markers for seed protein content in pigeonpea. Mol Gen Genom 294:57–68

  21. Perez-Fons L, Wells T, Corol DI, Ward JL, Gerrish C, Beale MH et al (2014) A genome-wide metabolomic resource for tomato fruit from Solanum pennellii. Sci Rep 4:3859

  22. Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L, Deal K, Luo M, Kong X, Bariana H, Mago R, McIntosh R, Dodds P, Dvorak J, Lagudah E (2013) The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341:786–788

  23. Qiu X, Chen K, Lv W, Ou X, Zhu Y, Xing D, Yang L, Fan F, Yang J, Xu J, Zheng T, Li Z (2017) Examining two sets of introgression lines reveals background-independent and stably expressed QTL that improve grain appearance quality in rice (Oryza sativa L.). Theor Appl Genet 130:951–967

  24. Rousseaux MC, Jones CM, Adams D, Chetelat R, Bennett A, Powell A (2005) QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor Appl Genet 111:1396–1408

  25. Saxena KB, Kumar RV, Srivastava N, Bao S (2005) A cytoplasmic-nuclear male-sterility system derived from a cross between Cajanus cajanifolius and Cajanus cajan. Euphytica 145:289–294

  26. Saxena RK, Penmetsa RV, Upadhyaya HD, Kumar A, Carrasquilla-Garcia N, Schlueter JA, Farmer A, Whaley AM, Sarma BK, May GD, Cook DR, Varshney RK (2012) Large-scale development of cost-effective SNP marker assays for genetic mapping in pigeonpea and comparative mapping in legumes. DNA Res 19:449–461

  27. Saxena RK, von Wettberg E, Upadhyaya HD, Sanchez V, Songok S, Saxena KB, Kimurto P, Varshney RK (2014) Genetic diversity and demographic history of Cajanus spp. Illustrated from genome-wide SNPs. PLoS ONE 9:e88568

  28. Saxena RK, Saxena KB, Pazhamala LT, Patel K, Parupalli S, Sameerkumar CV, Varshney RK (2015) Genomics for greater efficiency in pigeonpea hybrid breeding. Front Plant Sci 6:793

  29. Saxena RK, Kale SM, Kumar V, Parupalli S, Joshi S, Singh VK, Garg V, Das RR, Sharma M, Yamini KN, Ghanta A, Rathore A, Sameer Kumar CV, Saxena KB, Varshney RK (2017a) Genotyping-by sequencing of three mapping populations for identification of candidate genomic regions for resistance to sterility mosaic disease in pigeonpea. Sci Rep 7:1813

  30. Saxena RK, Obala J, Sinjushin A, Sameer Kumar CV, Saxena KB, Varshney RK (2017b) Characterization and mapping of Dt1 locus which co-segregates with CcTFL1 for growth habit in pigeonpea. Theor Appl Genet 130:1773–1784ss

  31. Saxena RK, Singh VK, Kale SM, Tathineni R, Parupalli S, Kumar V, Garg V, Das RR, Sharma M, Yamini KN, Muniswamy S, Ghanta A, Rathore A, Sameer Kumar CV, Saxena KB, Kavi Kishor PB, Varshney RK (2017c) Construction of genotyping-by-sequencing based high-density genetic maps and QTL mapping for fusarium wilt resistance in pigeonpea. Sci Rep 7:1911

  32. Saxena KB, Saxena RK, Sharma S, Sameer Kumar CV, Sultana R, von Wettberg EB, Varshney RK (2018a) The drivers and methodologies for exploiting wild Cajanus genome in pigeonpea breeding. Euphytica 214:222

  33. Saxena RK, Patel K, Sameer Kumar CV, Tyagi K, Saxena KB, Varshney RK (2018b) Molecular mapping and inheritance of restoration of fertility (Rf) in A4 hybrid system in pigeonpea (Cajanus cajan (L.) Millsp.). Theor Appl Genet 131:1605–1614

  34. Saxena RK, Rathore A, Bohra A, Yadav P, Das RR, Khan AW, Singh VK, Chitikineni A, Singh IP, Sameer Kumar CV, Saxena KB, Varshney RK (2018c) Development and application of high density Axiom®CajanusSNP Array with 56K SNPs to understand the genome architecture of released cultivars and founder genotypes for redefining future pigeonpea breeding programs. Plant Genome 11:180005. https://doi.org/10.3835/plantgenome2018.01.0005

  35. Schauer N, Semel Y, Roessner U et al (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24:447–454

  36. Schmalenbach I, Pillen K (2009) Detection and verification of malting quality QTLs using wild barley introgression lines. Theor Appl Genet 118:1411–1427

  37. Schmalenbach I, Leon J, Pillen K (2009) Identification and verification of QTLs for agronomic traits using wild barley introgression lines. Theor Appl Genet 118:483–497

  38. Sharma S (2017) Prebreeding using wild species for genetic enhancement of grain legumes at ICRISAT. Crop Sci 57:1132–1144

  39. Sharma S, Upadhyaya (2016) Interspecific hybridization to introduce useful genetic variability for pigeonpea improvement. Ind J Genet 76:496–503

  40. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806

  41. Subudhi PK, De Leon T, Singh PK, Parco A, Cohn MA, Sasaki T (2015) A chromosome segment substitution library of weedy rice for genetic dissection of complex agronomic and domestication traits. PLoS ONE 10:e0130650

  42. Swamy BP, Kaladhar K, Shobha Rani N, Prasad GS, Viraktamath BC, Reddy GA, Sarla N (2012) QTL analysis for grain quality traits in 2 BC2F2 populations derived from crosses between Oryza sativa cv Swarna and 2 accessions of O. nivara. J Hered 103:442–452

  43. Swarts K, Li H, Romero Navarro JA, An D, Romay MC, Hearne S et al (2014) Novel methods to optimize genotypic imputation for low-coverage, next-generation sequence data in crop plants. Plant Genome. https://doi.org/10.3835/plantgenome2014.05.0023

  44. Tanksley SD, Nelson JC (1996) Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Theor Appl Genet 92:191–203

  45. Thomson MJ, Edwards JD, Septiningsih EM, Harrington SE, McCouch SR (2006) Substitution mapping of dth1.1, a flowering-time quantitative trait locus (QTL) associated with transgressive variation in rice, reveals multiple sub-QTL. Genetics 172:2501–2514

  46. van der Maesen LJG (1986) Cajanus DC and Alylosia W. & A (Leguminosae). Agricultural University Wageningen papers 85-4 (1985). Agricultural University Wageningen, the Netherlands, p 222

  47. van der Maesen LJG (1990) Pigeonpea: origin, history, evolution and taxonomy. In: Nene YL, Hall SD, Sheila VK (eds) The pigeonpea. CAB International, Wallingford, pp 44–86

  48. Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MTA, Azam S, Fan G, Whaley AM, Farmer AD, Sheridan J, Iwata A, Tuteja R, Penmetsa RV, Wu W, Upadhyaya HD, Yang SP, Shah T, Saxena KB, Michael T, McCombie WR, Yang B, Zhang G, Yang H, Wang J, Spillane C, Cook DR, May GD, Xu X, Jackson SA (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol 30:83–89

  49. Varshney RK, Saxena RK, Upadhyaya HD, Khan AW, Yu Y, Kim C, Rathore A, Kim D, Kim J, An S, Kumar V, Anuradha G, Yamini KN, Zhang W, Muniswamy S, Kim JS, Penmetsa RV, von Wettberg EB, Datta SK (2017) Whole-genome resequencing of 292 pigeonpea accessions identifies genomic regions associated with domestication and agronomic traits. Nat Genet 49:1082–1088

  50. von Korff M, Wang H, Leon J, Pillen K (2006) AB-QTL analysis in spring barley: II Detection of favourable exotic alleles for agronomic traits introgressed from wild barley (H. vulgare ssp. spontaneum). Theor Appl Genet 112:1221–1231

  51. VSN International (2017) Genstat for Windows, 19th edn. VSN International, Hemel Hempstead, UK. Web page: Genstat.co.uk

  52. Wan XY, Wan JM, Jiang L, Wang JK, Zhai HQ, Weng JF, Wang HL, Lei CL, Wang JL, Zhang X, Cheng ZJ, Guo XP (2006) QTL analysis for rice grain length and fine mapping of an identified QTL with stable and major effects. Theor Appl Genet 112:1258–1270

  53. Wan X, Weng J, Zhai H, Wang J, Lei C, Liu X, Guo T, Jiang L, Su N, Wan J (2008) Quantitative trait loci (QTL) analysis for rice grain width and fine mapping of an identified QTL allele gw-5 in a recombination hotspot region on chromosome 5. Genet 179:2239–2252

  54. Wang ZY, Second G, Tanksley SD (1992) Polymorphism and phylogenetic relationships among species in the genus Oryza as determined by analysis of nuclear RFLPs. Theor Appl Genet 83:565–581

  55. Wang J, Wan X, Li H, Pfeiffer W, Crouch J, Wan J (2007) Application of identified QTL-marker associations in rice quality improvement through a design-breeding approach. Theor Appl Genet 115:87–100

  56. Xu Y, Zhu L, Xiao J, Huang N, McCouch SR (1997) Chromosomal regions associated with segregation distortion of molecular markers in F2, backcross, doubled haploid, and recombinant inbred populations in rice (Oryza sativa L.). Mol Gen Genet 253:535–545

  57. Xu J, Zhao Q, Du P, Xu C, Wang B, Feng Q, Liu Q, Tang S, Gu M, Han B, Liang G (2010) Developing high throughput genotyped chromosome segment substitution lines based on population whole-genome re-sequencing in rice (Oryza sativa L.). BMC Genom 11:656

  58. Yadav P, Saxena KB, Hingane A, Kumar CV, Kandalkar VS, Varshney RK, Saxena RK (2019) An “Axiom Cajanus SNP Array” based high density genetic map and QTL mapping for high-selfing flower and seed quality traits in pigeonpea. BMC Genom 20:235

  59. Yang SY, Saxena RK, Kulwal PL, Ash GJ, Dubey A, Harpe JDI, Upadhyaya HD, Gothalwal R, Kilian A, Varshney RK (2011) The first genetic map of pigeonpea based on Diversity Arrays Technology (DArT) markers. J Genet 90:103–109

  60. Yun SJ, Gyenis L, Bossolini E, Hayes PM, Matus I, Smith KP, Steffenson BJ, Tuberosa R, Muehlbauer GJ (2006) validation of quantitative trait loci for multiple disease resistance in barley using advanced backcross lines developed with a wild barley. Crop Sci 46:1179–1186

  61. Zamir D (2001) Improving plant breeding with exotic genetic libraries. Nat Rev Genet 2:983–989

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Acknowledgement

Authors are thankful for the Department of Agriculture Cooperation & Farmers’ Welfare, Ministry of Agriculture & Farmers Welfare, Government of India and United States Agency for International Development (USAID). This work is also partially funded as part of the initiative “Adapting Agriculture to Climate Change: Collecting, Protecting and Preparing Crop Wild Relatives,” which is supported by the Government of Norway. The project is managed by the Global Crop Diversity Trust. This work has been undertaken as part of the CGIAR Research Program on Grain Legumes and Dryland Cereals (GLDC). ICRISAT is a member of CGIAR Consortium.

Author information

RKV, RRM and RKS designed the experiments; NM led and RKV, RRM and RKS contributed to develop backcross populations; CVSK, NM, MS, AG, YN and RKS generated phenotyping data; RKV, RKS and SK generated genotyping data; RRD and AR analysed the phenotyping data; SK, PY, JM analysed the genotyping data and performed QTL analysis with support of RKS and RKV. All authors reviewed and approved the submission.

Correspondence to Rajeev K. Varshney.

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Saxena, R.K., Kale, S., Mir, R.R. et al. Genotyping-by-sequencing and multilocation evaluation of two interspecific backcross populations identify QTLs for yield-related traits in pigeonpea. Theor Appl Genet 133, 737–749 (2020). https://doi.org/10.1007/s00122-019-03504-z

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