High-resolution skim genotyping by sequencing reveals the distribution of crossovers and gene conversions in Cicer arietinum and Brassica napus

Abstract

Key message

We characterise the distribution of crossover and non-crossover recombination in Brassica napus and Cicer arietinum using a low-coverage genotyping by sequencing pipeline SkimGBS.

Abstract

The growth of next-generation DNA sequencing technologies has led to a rapid increase in sequence-based genotyping for applications including diversity assessment, genome structure validation and gene–trait association. We have established a skim-based genotyping by sequencing method for crop plants and applied this approach to genotype-segregating populations of Brassica napus and Cicer arietinum. Comparison of progeny genotypes with those of the parental individuals allowed the identification of crossover and non-crossover (gene conversion) events. Our results identify the positions of recombination events with high resolution, permitting the mapping and frequency assessment of recombination in segregating populations.

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References

  1. Bus A, Hecht J, Huettel B, Reinhardt R, Stich B (2012) High-throughput polymorphism detection and genotyping in Brassica napus using next-generation RAD sequencing. BMC Genom 13:281

    Article  CAS  Google Scholar 

  2. Chalhoub B et al (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953. doi:10.1126/science.1253435

    Article  CAS  PubMed  Google Scholar 

  3. Chen JM, Cooper DN, Chuzhanova N, Ferec C, Patrinos GP (2007) Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet 8:762–775. doi:10.1038/nrg2193

    Article  CAS  PubMed  Google Scholar 

  4. Cheng F, Mandakova T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the Mesohexaploid Brassica rapa. Plant Cell 25:1541–1554. doi:10.1105/tpc.113.110486

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Drouaud J et al (2013) Contrasted patterns of crossover and non-crossover at Arabidopsis thaliana meiotic recombination hotspots. PLoS Genet 9:e1003922. doi:10.1371/journal.pgen.1003922

    Article  PubMed Central  PubMed  Google Scholar 

  6. Edwards D, Batley J (2010) Plant genome sequencing: applications for crop improvement. Plant Biotechnol J 8:2–9. doi:10.1111/j.1467-7652.2009.00459.x

    Article  CAS  PubMed  Google Scholar 

  7. Edwards D, Batley J, Snowdon RJ (2013) Accessing complex crop genomes with next-generation sequencing. Theor Appl Genet 126:1–11. doi:10.1007/s00122-012-1964-x

    Article  CAS  PubMed  Google Scholar 

  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. doi:10.1371/journal.pone.0019379

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Farkhari M, Lu Y, Shah T, Zhang S, Naghavi MR, Rong T, Xu Y (2011) Recombination frequency variation in maize as revealed by genomewide single-nucleotide polymorphisms. Plant Breed 130:533–539

    Article  CAS  Google Scholar 

  10. Gaur R et al (2012) High-throughput SNP discovery and genotyping for constructing a saturated linkage map of chickpea (Cicer arietinum L.). DNA Res 19:357–373. doi:10.1093/dnares/dss018

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Gaut BS, Wright SI, Rizzon C, Dvorak J, Anderson LK (2007) Recombination: an underappreciated factor in the evolution of plant genomes. Nat Rev Genet 8:77–84. doi:10.1038/nrg1970

    Article  CAS  PubMed  Google Scholar 

  12. Hayward A, Mason A, Dalton-Morgan J, Zander M, Edwards D, Batley J (2012a) SNP discovery and applications in Brassica napus. J Plant Biotechnol 39:1–12

    Article  Google Scholar 

  13. Hayward A et al (2012b) Second-generation sequencing for gene discovery in the Brassicaceae. Plant Biotechnol J 10:750–759. doi:10.1111/j.1467-7652.2012.00719.x

    Article  CAS  PubMed  Google Scholar 

  14. Helms C et al (1992) Closure of a genetic linkage map of human chromosome 7q with centromere and telomere polymorphisms. Genomics 14:1041–1054

    Article  CAS  PubMed  Google Scholar 

  15. Jain M et al (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729. doi:10.1111/tpj.12173

    Article  CAS  PubMed  Google Scholar 

  16. Lai K et al (2014) Identification and characterization of more than 4 million intervarietal SNPs across the group 7 chromosomes of bread wheat. Plant Biotechnol J 13:97–104. doi:10.1111/pbi.12240

    Article  PubMed  Google Scholar 

  17. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967. doi:10.1093/bioinformatics/btp336

    Article  CAS  PubMed  Google Scholar 

  18. Liu S et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930. doi:10.1038/ncomms4930

    PubMed Central  CAS  PubMed  Google Scholar 

  19. Lorenc M et al (2012) Discovery of single nucleotide polymorphisms in complex genomes using SGSautoSNP. Biology 1:370–382. doi:10.3390/biology1020370

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Mezard C, Vignard J, Drouaud J, Mercier R (2007) The road to crossovers: plants have their say. Trends Genet 23:91–99. doi:10.1016/j.tig.2006.12.007

    Article  CAS  PubMed  Google Scholar 

  21. Parkin IA et al (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol 15:R77. doi:10.1186/gb-2014-15-6-r77

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Qi J, Chen Y, Copenhaver GP, Ma H (2014) Detection of genomic variations and DNA polymorphisms and impact on analysis of meiotic recombination and genetic mapping. Proc Natl Acad Sci USA 111:10007–10012. doi:10.1073/pnas.1321897111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Qiu D et al (2006) A comparative linkage map of oilseed rape and its use for QTL analysis of seed oil and erucic acid content. Theor Appl Genet 114:67–80. doi:10.1007/s00122-006-0411-2

    Article  CAS  PubMed  Google Scholar 

  25. Roberts PA (1965) Difference in behaviour of Eu- and Hetero-chromatin—crossing-over. Nature 205:725–726. doi:10.1038/205725b0

    Article  CAS  PubMed  Google Scholar 

  26. Ruperao P et al (2014) A chromosomal genomics approach to assess and validate the desi and kabuli draft chickpea genome assemblies. Plant Biotechnol J 12:778–786. doi:10.1111/pbi.12182

    Article  CAS  PubMed  Google Scholar 

  27. Sun Z, Wang Z, Tu J, Zhang J, Yu F, McVetty PB, Li G (2007) An ultradense genetic recombination map for Brassica napus, consisting of 13551 SRAP markers. Theor Appl Genet 114:1305–1317. doi:10.1007/s00122-006-0483-z

    Article  CAS  PubMed  Google Scholar 

  28. Varshney RK et al (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31:240–246. doi:10.1038/nbt.2491

    Article  CAS  PubMed  Google Scholar 

  29. Wang X et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039. doi:10.1038/ng.919

    Article  CAS  PubMed  Google Scholar 

  30. Wijnker E et al. (2013) The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. Elife 2: e01426 doi:10.7554/eLife.01426

  31. Yang S et al (2012) Great majority of recombination events in Arabidopsis are gene conversion events. Proc Natl Acad Sci USA 109:20992–20997. doi:10.1073/pnas.1211827110

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Yao H, Zhou Q, Li J, Smith H, Yandeau M, Nikolau BJ, Schnable PS (2002) Molecular characterization of meiotic recombination across the 140-kb multigenic a1-sh2 interval of maize. Proc Natl Acad Sci USA 99:6157–6162. doi:10.1073/pnas.082562199

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to acknowledge funding support from the Australian Research Council (Projects LP0882095, LP0883462, LP110100200 and DP0985953), the Australian India Strategic Research Fund (AISRF) Grand Challenge fund (GCF010013), CGIAR Generation Challenge Programme (Theme Leader Discretionary grant), the Australian Genome Research Facility (AGRF), the Queensland Cyber Infrastructure Foundation (QCIF) and the Australian Partnership for Advanced Computing (APAC) and the Center of Excellence in Genomics (CEG) of ICRISAT. The part of this work has been undertaken as part of the CGIAR Research Program on Grain Legumes. ICRISAT is a member of the CGIAR Consortium.

Conflict of interest

The authors declare no conflict of interest.

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Correspondence to David Edwards.

Additional information

All scripts used in this study are available at http://www.appliedbioinformatics.com.au/index.php/SkimGBS.

Communicated by L. Jiang.

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Bayer, P.E., Ruperao, P., Mason, A.S. et al. High-resolution skim genotyping by sequencing reveals the distribution of crossovers and gene conversions in Cicer arietinum and Brassica napus . Theor Appl Genet 128, 1039–1047 (2015). https://doi.org/10.1007/s00122-015-2488-y

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Keywords

  • Recombination Event
  • Gene Conversion
  • Genome Sequence Data
  • Cicer Arietinum
  • Gene Conversion Event