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Genetic diversity and population structure in Beninese pigeon pea [Cajanus cajan (L.) Huth] landraces collection revealed by SSR and genome wide SNP markers

Genetic Resources and Crop Evolution volume 67, pages 191–208 (2020)Cite this article

Abstract

Pigeon pea [Cajanus cajan (L.) Huth] is a valuable multipurpose crop locally used for household food security as well in traditional medicine in Benin. However, due to the neglected status of the crop, its genetic resources are not well evaluated and its agronomic potential remains undetermined. For breeding purpose, a total of 77 landraces from Benin and three breeding lines were simultaneously genotyped with 30 preselected SSRs and 794 GBS derived SNPs in order to estimate the genetic diversity and infer the population structure within the collection. Both marker types were found informative in polymorphism analysis revealing all high genetic variability. The 30 SSR markers led to a total of 209 alleles with an average of 6.97 alleles per locus, whereas only biallelic SNPs were extracted from GBS data according to specific filter criteria. The polymorphism information content value was 0.57 and 0.25 for SSR and SNP, respectively. The genetic diversity calculated as expected heterozygosity was higher for SSR (0.62) than for SNP (0.35). The inference of the genetic structure subdivided the entire collection into three major groups independent of the marker type. However, the resolving power in population structure analysis was higher for SNP than for SSR. AMOVA and PCoA analyses showed clearer population structure with SNP than SSR. The present study provides a clear insight on the genetic diversity in Beninese pigeon pea and represents the first report comparing the performance of SSR and SNP markers for population genetics analysis in cultivated pigeon pea. It provides useful information for further pigeon pea conservation and breeding in Benin.

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References

  • Abrol DP, Shankar U (2015) Role of pollination in pulses. Adv Pollen Spore Res 33:101–103

    Google Scholar 

  • Adoukonou-Sagbadja H, Wagner C, Dansi A, Ahlemeyer J, Daïnou O, Akpagana K, Ordon F, Friedt W (2007) Genetic diversity and population differentiation of traditional fonio millet (Digitaria spp.) landraces from different agroecological zones of West Africa. Theor Appl Genet 115:917–931

    PubMed  CAS  Google Scholar 

  • Ae N, Arihara J, Okada K, YoshiharaT JC (1990) Phosphorous uptake by pigeon pea and its role in cropping systems of the Indian subcontinent. Science 248:477–480

    PubMed  CAS  Google Scholar 

  • Ayenan MAT, Danquah A, Ahoton LE, Ofori K (2017a) Utilization and farmers’ knowledge on pigeon pea diversity in Benin, West Africa. J Ethnobiol Ethnomed 13:37. https://doi.org/10.1186/s13002-017-0164-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Ayenan MAT, Ofori K, Ahoton LE, Danquah A (2017b) Pigeonpea [(Cajanus cajan (L.) Millsp.)] production system, farmers’ preferred traits and implications for variety development and introduction in Benin. Agric Food Secur 6:48. https://doi.org/10.1186/s40066-017-0129-1

    Article  Google Scholar 

  • Bengtsson T, The PPP Barley Consortium, Manninen O, Jahoor A, Orabi J (2017) Genetic diversity, population structure and linkage disequilibrium in Nordic spring barley (Hordeum vulgare L. subsp. vulgare). Genet Resour Crop Evol 64(8):2021–2033

    Google Scholar 

  • Bohra A, Dubey A, Saxena RK, Penmetsa RV, Poomima KN, Kumar N, Farmer AD, Srivani G, Upadhyaya HD, Gothalwal R, Ramesh S, Singh D, Saxena K, Kishor PBK, Singh KN, 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 pigeon pea (Cajanus spp.). BMC Plant Biol 11:56. https://doi.org/10.1186/1471-2229-11-56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bohra A, Saxena RK, Gnanesh BN, Saxena K, Byregowda M, Rathore A, KaviKishor PB, Cook DR, Varshney RK (2012) An intra-specific consensus genetic map of pigeon pea [Cajanus cajan (L.) Millspaugh] derived from six mapping populations. Theor Appl Genet 125:1325–1338

    PubMed  PubMed Central  Google Scholar 

  • Bohra A, Jha R, Pandey G, Patil PG, Saxena RK, Singh IP, Singh D, Mishra RK, Mishra A, Singh F, Varshney RK, Singh NP (2017) New hypervariable SSR markers for diversity analysis, Hybrid purity testing and trait mapping in pigeon pea [Cajanus cajan (L.) Millspaugh]. Front Plant Sci 8:377. https://doi.org/10.3389/fpls.2017.00377

    Article  PubMed  PubMed Central  Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of genetic linkage map in man using restriction fragment length polymorphism. Am J Hum Genet 32(3):314–331

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chen W, Hou L, Zhang Z, Pang X, Li Y (2017) Genetic diversity, population structure, and linkage disequilibrium of a core collection of Ziziphus jujuba assessed with genome-wide SNPs developed by genotyping-by-sequencing and SSR markers. Front Plant Sci 8:575. https://doi.org/10.3389/fpls.2017.00575

    Article  PubMed  PubMed Central  Google Scholar 

  • Dansi A, Vodouhe R, Azokpota P, Yedomonhan H, Assogba P, Adjatin A, Dossou-Aminon I, Akpagana K (2012) Diversity of the neglected and underutilized crop species of importance in Benin. Sci World J. https://doi.org/10.1100/2012/932947

    Article  Google Scholar 

  • Desalegne BA, Dagne K, Melaku G, Ousmane B, Fatokun CA (2017) Efficiency of SNP and SSR-based analysis of genetic diversity, population structure, and relationships among Cowpea (Vigna unguiculata (L.) Walp.) germplasm from East Africa and IITA Inbred Lines. J Crop Sci Biotechnol 20(2):107–128

    Google Scholar 

  • Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361

    Google Scholar 

  • Emanuelli F, Lorenzi S, Grzeskowiak L, Catalano V, Stefanini M, Troggio M, Myles S, Martinez-Zapater JM, Zyprian E, Moreira FM, Grando MS (2013) Genetic diversity and population structure assessed by SSR and SNP markers in a large germplasm collection of grape. BMC Plant Biol 13:39. https://doi.org/10.1186/1471-2229-13-39

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    PubMed  CAS  Google Scholar 

  • Filipi CV, Aguirre N, Rivas JG, Zubrzycki J, Puebla A, Cordes D, Moreno MV, Fusari CM, Avarez D, Heinz RA, Hopp HE, Paniego NB, Lia VV (2015) Population structure and genetic diversity characterization of a sunflower association mapping population using SSR and SNP markers. BMC Plant Biol 15:52. https://doi.org/10.1186/s12870-014-0360-x

    Article  CAS  Google Scholar 

  • Gupta PK, Varshney RK (2000) The development and use of microsatellite markers for genetic analysis and plant breeding with emphasis on bread wheat. Euphytica 13:163–185

    Google Scholar 

  • Gupta V, Dorsey G, Hubbard AE, Rosenthal PJ, Greenhouse B (2010) Gel versus capillary electrophoresis genotyping for categorizing treatment outcomes in two anti-malarial trials in Uganda. Malar J 9:19. https://doi.org/10.1186/1475-2875-9-19

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hamblin MT, Warburton ML, Buckler ES (2007) Empirical comparison of simple sequence repeats and single nucleotide polymorphisms in assessment of maize diversity and relatedness. PLoS ONE 2:e1367. https://doi.org/10.1371/journal.pone.0001367

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kassa MT, Penmetsa RV, Carraquille-Garde N, Sarma BK, Datta S, Upadhyaya HD, Varshney RK, von Wettberg EJB, Cook DR (2012) Genetic patterns of domestication in pigeon pea (Cajanus cajan (L.) Millsp) and wild Cajanus relatives. PLoS ONE 7(6):e39563. https://doi.org/10.1371/journal.pone.0039563

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar A, Priyanka VL, Lall V, Lal D (2011) A biotic factors and pigeon pea pod fly, Melanagromyza Obtusa (Malloch). Indian J Entomol 73:59–62

    Google Scholar 

  • 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(8):1673–1681

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kumawat G, Raje RS, Bhutani S, Pal JK, Mithra ASVCR, Gaikwad K, Sharma TR et al (2012) Molecular mapping of QTLs for plant type and earliness traits in pigeon pea (Cajanus cajan L. Millsp.). BMC Genet 13:84. https://doi.org/10.1186/1471-2156-13-84

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis G, Schrire B, MacKinder B, Lock M (2005) Legumes of the world. Royal Botanic Gardens, Kew Publishing, London

    Google Scholar 

  • Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714

    CAS  PubMed  Google Scholar 

  • Li YH, Li W, Zhang C, Yang L, Chang RZ, Gaut BS et al (2010) Genetic diversity in domesticated soybean (Glycine max) and its wild progenitor (Glycine soja) for simple sequence repeat and single-nucleotide polymorphism loci. New Phytol 188:242–253

    PubMed  CAS  Google Scholar 

  • Liu KJ, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129

    PubMed  CAS  Google Scholar 

  • Martinez-Arias R, Calafell F, Mateu E, Comas D, Andres A, Bertranpetit J (2001) Sequence variability of a human pseudogene. Genome Res 11(6):1071–1085

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mir RR, Varshney RK (2013) Future prospects of molecular markers in plants. In: Henry RJ (ed) Molecular markers in plants. Blackwell, Oxford, pp 170–190

    Google Scholar 

  • Mir RR, Kudapa H, Srikanth S, Saxena RK, Sharma A, Azam S, Saxena K, Penmetsa RV, Varshney RK (2014) Candidate gene analysis for determinacy in pigeon pea (Cajanus spp.). Theor Appl Genet 127:2663–2678

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mohamed A, García-Martínez S, Loumerem M, Carbonell P, Ruiz JJ, Boubaker M (2019) Assessment of genetic diversity among local pea (Pisum sativum L.) accessions cultivated in the arid regions of Southern Tunisia using agro-morphological and SSR molecular markers. Genet Resour Crop Evol 66:1189–1203. https://doi.org/10.1007/s10722-019-00784-8

    Article  CAS  Google Scholar 

  • Njung’e V, Deshpande S, Siambi M, Jones R, Silim S, De Villiers S (2016) SSR genetic diversity assessment of popular pigeon pea varieties in Malawi reveals unique fingerprints. Electron J Biotechnol 21:65–71

    Google Scholar 

  • Odeny AD (2006) Microsatellite development and application in Pigeon pea (Cajanus cajan (L.) Millsp). Ph.D. Dissertation, Bonn

  • Odeny DA, Jayashree B, Ferguson M, Hoisington D, Crouch J, Gebhardt C (2007) Development, characterization and utilization of microsatellite markers in pigeon pea. Plant Breed 126:130–136

    CAS  Google Scholar 

  • Odeny DA, Shah T, Saxena RK (2016) Genomic resources for pigeon pea. Legumes Perspect 11:33–34

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    PubMed  PubMed Central  CAS  Google Scholar 

  • Perovic J, Silvar C, Koenig J, Stein N, Perovic D, Ordon F (2013) A versatile fluorescence-based multiplexing assay for CAPS genotyping on capillary electrophoresis systems. Mol Breed 32:61–69

    CAS  Google Scholar 

  • Petchiammal KI, Muthiah AR, Jayamani P (2015) Molecular characterization of CGMS, maintainer and inbred lines and diversity analysis in pigeon pea [Cajanus cajan (L.) Millsp.]. Legume Res 38(2):734–741

    Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7(2):e32253. https://doi.org/10.1371/journal.pone.0032253

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181

    PubMed  PubMed Central  CAS  Google Scholar 

  • Reddy LJ (1990) Pigeonpea: morphology. The pigeon pea. CAB International, Wallingford, Oxon, pp 47–88

    Google Scholar 

  • Saxena KB, Singh L, Gupta MD (1990) Variation for natural out-crossing in pigeon pea. Euphytica 46:143–148

    Google Scholar 

  • Saxena RK, von Wettberg E, Upadhyaya HD, Sanchez V, Songok S, Saxena K, Kimurto P, Varshney RK (2014) Genetic diversity and demographic history of Cajanus spp. illustrated from genome-wide SNPs. PLoS ONE 9(2):e88568. https://doi.org/10.1371/journal.pone.0088568

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saxena RK, Saxena KB, Pazhamala LT, Patel K, Parupalli S, Sameerkumar CV, Varshney RK (2015) Genomics for greater efficiency in pigeon pea hybrid breeding. Front Plant Sci. 6:793. https://doi.org/10.3389/fpls.2015.00793

    Article  PubMed  PubMed Central  Google Scholar 

  • Saxena RK, Kale SM, Kumar V, Parupali S, Joshi S, Singh V, Garg V, Das RR, Sharma M, Yamini KN, Ghanta A, Rathore A, Sameerkumar CV, Saxena KB, Varshney RK (2017) Genotyping-by-sequencing of three mapping populations for identification of candidate genomic regions for resistance to sterility mosaic disease in pigeon pea. Sci Rep 7(1):1813. https://doi.org/10.1038/s41598-017-01535-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma S, Agarwal N, Verma P (2011) Pigeon pea (Cajanus cajan L.): a hidden treasure of regime nutrition. J Funct Environ Bot 1(2):91–101

    Google Scholar 

  • Sharma M, Ghosh R, Telangre R, Rathore A, Saifulla M, Mahalinga DM, Saxena DR, Jain YK (2016) Environmental influences on Pigeonpea–Fusarium udum interactions and stability of genotypes to Fusarium Wilt. Front Plant Sci 7:253. https://doi.org/10.3389/fpls.2016.00253

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh N, Tyagi RK, Pandey C (2013) Genetic resources of pigeon pea: conservation for use. National Bureau of Plant Genetic Resources (NBPGR), New Delhi, pp 1–49

    Google Scholar 

  • Singh N, Choudhury DR, Singh AK, Kumar S, Srinivasan K et al (2013) Comparison of SSR and SNP markers in estimation of genetic diversity and population structure of Indian rice varieties. PLoS ONE 8(12):e84136. https://doi.org/10.1371/journal.pone.0084136

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soto-Cerda BJ, Maureira-Butler I, Munoz G, Rupayan A, Cloutier S (2012) SSR-based population structure, molecular diversity and linkage disequilibrium analysis of a collection of flax (Linum usitatissimum L.) varying for mucilage seed-coat content. Mol Breeding 30:875–888

    Google Scholar 

  • Sousa ACB, Godoy R, Sforça DA, de Campos T, Zucchi MI, Jank L, de Sousa AP (2011) Genetic diversity analysis among pigeon pea genotypes adapted to South American regions based on microsatellites markers. Sci Agric 68(4):431–439

    Google Scholar 

  • Stein N, Herren G, Beat K (2001) A new DNA extraction method for high-throughput marker analysis in a large-genome species such as Triticum saetivum. Plant Breed 120(4):354–356

    CAS  Google Scholar 

  • Van der Maesen LJG (1990) Pigeon pea: origin, history, evolution, and taxonomy. In: Nene YH, Hall SD, Sheila VK (eds) The pigeon pea. CAB International, Wallingford, pp 15–46

    Google Scholar 

  • Varshney RK, Penmetsa RV, Dutta S, Kulwal PL, Saxena RK, Datta S, Sharma TR, Rosen B, Carrasquilla-Garcia N et al (2010) Pigeon pea genomics initiative (PGI): an international effort to improve crop productivity of pigeon pea (Cajanus cajan L.). Mol Breeding 26:393–408

    CAS  Google Scholar 

  • Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MT et al (2012) Draft genome sequence of pigeon pea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol 30:83–89

    CAS  Google Scholar 

  • Varshney RK, Mohan SM, Gaur PM, Gangarao NVPR, Pandey MK, Bohra A et al (2013) Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnol Adv 31:1120–1134

    PubMed  Google Scholar 

  • Varshney RK, Saxena RK, Upadhyaya HD, Khan AW, Yu Y, Kim C et al (2017) Whole-genome resequencing of 292 pigeon pea accessions identifies genomic regions associated with domestication and agronomic traits. Nat Genet 49(7):1082–1088

    PubMed  CAS  Google Scholar 

  • Wendler N, Mascher M, Noh C, Himmelbach A, Scholz U, Ruge-Wehling B, Stein N (2014) Unlocking the secondary gene-pool of barley with next-generation sequencing. Plant Biotechnol J 12:1122–1131

    PubMed  CAS  Google Scholar 

  • Wurschum T, Langer SM, Friedrich C, Longin H, Korzun V, Akhunov E, Ebmeyer E, Schachschneider R, Schacht J, Kazman E, Reif JC (2013) Population structure, genetic diversity and linkage disequilibrium in elite winter wheat assessed with SNP and SSR markers. Theor Appl Genet 126(6):1477–1486

    PubMed  Google Scholar 

  • Yang S, Pang W, Harper J, Carling J, Wenzl P, Huttner E et al (2006) Low level of genetic diversity in cultivated pigeon pea compared to its wild relatives is revealed by diversity arrays technology (DArT). Theor Appl Genet 113:585–595

    PubMed  CAS  Google Scholar 

  • Zavinon F, Adoukonou-Sagbadja H, Ahoton L, Vodouhê R, Ahanhanzo C (2018) Quantitative analysis, distribution and traditional management of pigeon pea [Cajanus cajan (L.) Millsp.] landraces’ diversity in Southern Benin. Eur Sci J 14(9):184–211

    Google Scholar 

  • Zavinon F, Adoukonou-Sagbadja H, Bossipkonnon A, Dossa H, Corneille A (2019) Phenotypic diversity for agro-morphological traits in pigeon pea landraces [(Cajanus cajan L.) Millsp.] cultivated in southern Benin. Open Agric 4:487–499

    Google Scholar 

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Acknowledgements

Fiacre Zavinon thanks DAAD for financial support and Dr. Rajeev Varshney from ICRISAT for help in selecting SSR markers used in this study. Special thanks to Katy Niedung, Marlis Weilepp and Thomas Berner for technical assistance. The authors extend also special thanks to Ayenan Mathieu for supplying a part of analyzed plant material and the two anonymous reviewers for their critical comments.

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Authors and Affiliations

  1. Laboratory of Genetic Resources and Molecular Breeding (LaREGAME), Department of Genetic and Biotechnology, Faculty of Sciences and Techniques, University of Abomey-Calavi, BP 1947, Abomey-Calavi, Republic of Benin

    Fiacre Zavinon & Hubert Adoukonou-Sagbadja

  2. Institute for Resistance Research and Stress Tolerance, Federal Research Centre for Cultivated Plants, Julius Kühn-Institut (JKI), Erwin-Baur-Str. 27, 06484, Quedlinburg, Saxony-Anhalt, Germany

    Fiacre Zavinon, Frank Ordon & Dragan Perovic

  3. Institute for Biosafety in Plant Biotechnology, Federal Research Centre for Cultivated Plants, Julius Kühn-Institut (JKI), Erwin-Baur-Str. 27, 06484, Quedlinburg, Saxony-Anhalt, Germany

    Jens Keilwagen & Heike Lehnert

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  1. Fiacre Zavinon
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  2. Hubert Adoukonou-Sagbadja
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Correspondence to Hubert Adoukonou-Sagbadja.

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Zavinon, F., Adoukonou-Sagbadja, H., Keilwagen, J. et al. Genetic diversity and population structure in Beninese pigeon pea [Cajanus cajan (L.) Huth] landraces collection revealed by SSR and genome wide SNP markers. Genet Resour Crop Evol 67, 191–208 (2020). https://doi.org/10.1007/s10722-019-00864-9

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Keywords

  • Benin
  • Genetic diversity
  • Pigeon pea
  • Population structure
  • Single nucleotide polymorphisms (SNP)
  • Simple sequence repeat (SSR)