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Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel

Abstract

Arabidopsis thaliana is native to Eurasia and is naturalized across the world. Its ability to be easily propagated and its high phenotypic variability make it an ideal model system for functional, ecological and evolutionary genetics. To date, analyses of the natural genetic variation of A. thaliana have involved small numbers of individual plants or genetic markers. Here we genotype 1,307 worldwide accessions, including several regional samples, using a 250K SNP chip. This allowed us to produce a high-resolution description of the global pattern of genetic variation. We applied three complementary selection tests and identified new targets of selection. Further, we characterized the pattern of historical recombination in A. thaliana and observed an enrichment of hotspots in its intergenic regions and repetitive DNA, which is consistent with the pattern that is observed for humans but which is strikingly different from that observed in other plant species. We have made the seeds we used to produce this Regional Mapping (RegMap) panel publicly available. This panel comprises one of the largest genomic mapping resources currently available for global natural isolates of a non-human species.

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Figure 1: PCA of the study samples.
Figure 2: Recombination rate variation for chromosome 1.
Figure 3: The proportion of DNA within and outside of inferred hotspots.
Figure 4: Overlap of selection scans with results from GWAS on chromosome 2.
Figure 5: Enrichment of GWAS results with signals of selection.

References

  1. Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627–631 (2010).

    Article  CAS  Google Scholar 

  2. Brachi, B. et al. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet. 6, e1000940 (2010).

    Article  Google Scholar 

  3. Li, Y., Huang, Y., Bergelson, J., Nordborg, M. & Borevitz, J.O. Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 107, 21199–21204 (2010).

    Article  CAS  Google Scholar 

  4. Baxter, I. et al. A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLoS Genet. 6, e1001193 (2010).

    Article  Google Scholar 

  5. Kim, S. et al. Recombination and linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 39, 1151–1155 (2007).

    Article  CAS  Google Scholar 

  6. Clark, R.M. et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338–342 (2007).

    Article  CAS  Google Scholar 

  7. Patterson, N., Price, A.L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).

    Article  Google Scholar 

  8. Nordborg, M. et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196 (2005).

    Article  Google Scholar 

  9. Platt, A. et al. The scale of population structure in Arabidopsis thaliana. PLoS Genet. 6, e1000843 (2010).

    Article  Google Scholar 

  10. Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43, 956–963 (2011).

    Article  CAS  Google Scholar 

  11. Lewandowska-Sabat, A.M., Fjellheim, S. & Rognli, O.A. Extremely low genetic variability and highly structured local populations of Arabidopsis thaliana at higher latitudes. Mol. Ecol. 19, 4753–4764 (2010).

    Article  CAS  Google Scholar 

  12. McVean, G.A. et al. The fine-scale structure of recombination rate variation in the human genome. Science 304, 581–584 (2004).

    Article  CAS  Google Scholar 

  13. Bergthorsson, U., Andersson, D.I. & Roth, J.R. Ohno's dilemma: evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. USA 104, 17004–17009 (2007).

    Article  CAS  Google Scholar 

  14. Yang, S. et al. Repetitive element–mediated recombination as a mechanism for new gene origination in Drosophila. PLoS Genet. 4, e3 (2008).

    Article  Google Scholar 

  15. McDowell, J.M. et al. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10, 1861–1874 (1998).

    Article  CAS  Google Scholar 

  16. Yandeau-Nelson, M.D. et al. MuDR transposase increases the frequency of meiotic crossovers in the vicinity of a Mu insertion in the maize a1 gene. Genetics 169, 917–929 (2005).

    Article  CAS  Google Scholar 

  17. Hollister, J.D. & Gaut, B.S. Population and evolutionary dynamics of Helitron transposable elements in Arabidopsis thaliana. Mol. Biol. Evol. 24, 2515–2524 (2007).

    Article  CAS  Google Scholar 

  18. Hu, T.T. et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476–481 (2011).

    Article  Google Scholar 

  19. Myers, S., Freeman, C., Auton, A., Donnelly, P. & McVean, G. A common sequence motif associated with recombination hot spots and genome instability in humans. Nat. Genet. 40, 1124–1129 (2008).

    Article  CAS  Google Scholar 

  20. Myers, S., Bottolo, L., Freeman, C., McVean, G. & Donnelly, P. A fine-scale map of recombination rates and hotspots across the human genome. Science 310, 321–324 (2005).

    Article  CAS  Google Scholar 

  21. Gill, K.S., Gill, B.S., Endo, T.R. & Taylor, T. Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat. Genetics 144, 1883–1891 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Lichten, M. & Goldman, A.S. Meiotic recombination hotspots. Annu. Rev. Genet. 29, 423–444 (1995).

    Article  CAS  Google Scholar 

  23. Morgante, M., Hanafey, M. & Powell, W. Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat. Genet. 30, 194–200 (2002).

    Article  CAS  Google Scholar 

  24. Blanc, G. & Wolfe, K.H. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16, 1667–1678 (2004).

    Article  CAS  Google Scholar 

  25. Swigonová, Z. et al. Close split of sorghum and maize genome progenitors. Genome Res. 14, 1916–1923 (2004).

    Article  Google Scholar 

  26. SanMiguel, P., Gaut, B.S., Tikhonov, A., Nakajima, Y. & Bennetzen, J.L. The paleontology of intergene retrotransposons of maize. Nat. Genet. 20, 43–45 (1998).

    Article  CAS  Google Scholar 

  27. He, L. & Dooner, H.K. Haplotype structure strongly affects recombination in a maize genetic interval polymorphic for Helitron and retrotransposon insertions. Proc. Natl. Acad. Sci. USA 106, 8410–8416 (2009).

    Article  CAS  Google Scholar 

  28. Myers, S. et al. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327, 876–879 (2010).

    Article  CAS  Google Scholar 

  29. Hancock, A.M. et al. Adaptation to climate across the Arabidopsis thaliana genome. Science 334, 83–86 (2011).

    Article  CAS  Google Scholar 

  30. Fournier-Level, A. et al. A map of local adaptation in Arabidopsis thaliana. Science 334, 86–89 (2011).

    Article  CAS  Google Scholar 

  31. Smith, J.M. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23–35 (1974).

    Article  CAS  Google Scholar 

  32. Toomajian, C. et al. A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biol. 4, e137 (2006).

    Article  Google Scholar 

  33. Nielsen, R. et al. Genomic scans for selective sweeps using SNP data. Genome Res. 15, 1566–1575 (2005).

    Article  CAS  Google Scholar 

  34. Lewontin, R.C. & Krakauer, J. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74, 175–195 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Hartmann, U. et al. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351–360 (2000).

    Article  CAS  Google Scholar 

  36. Alonso-Blanco, C., Bentsink, L., Hanhart, C.J., Blankestijn-de Vries, H. & Koornneef, M. Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164, 711–729 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Chiang, G.C. et al. DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana. Mol. Ecol. 20, 3336–3349 (2011).

    Article  CAS  Google Scholar 

  38. Pritchard, J.K., Pickrell, J.K. & Coop, G. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr. Biol. 20, R208–R215 (2010).

    Article  CAS  Google Scholar 

  39. Lin, X. et al. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402, 761–768 (1999).

    Article  CAS  Google Scholar 

  40. Bakker, E.G., Traw, M.B., Toomajian, C., Kreitman, M. & Bergelson, J. Low levels of polymorphism in genes that control the activation of defense response in Arabidopsis thaliana. Genetics 178, 2031–2043 (2008).

    Article  CAS  Google Scholar 

  41. Bakker, E.G., Toomajian, C., Kreitman, M. & Bergelson, J. A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell 18, 1803–1818 (2006).

    Article  CAS  Google Scholar 

  42. Gan, X. et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419–423 (2011).

    Article  CAS  Google Scholar 

  43. Anastasio, A.E. et al. Source verification of misidentified Arabidopsis thaliana accessions. Plant J. 67, 554–566 (2011).

    Article  CAS  Google Scholar 

  44. Weir, B.S. & Cockerham, C.C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).

    CAS  Google Scholar 

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Acknowledgements

We thank M. Hubisz for the code for the CLR statistic and for help in using the software. We also thank E. Leffler for helpful discussions regarding recombination hotspots. M.W.H. was supported by a National Science Foundation Predoctoral Fellowship, a Graduate Assistance in Areas of National Need (GAANN) training grant and an Achievement Rewards for College Scientists (ARCS) Foundation Scholarship. This research was supported by US National Institutes of Health grant GM057994 (J.B.), US National Institutes of Health grant GM083068 (J.B. and M.N.), National Science Foundation 2010 grants (M.N. and J.B.) and a Dropkin Foundation Fellowship (A.M.H.). This is contribution number 11-363-J from the Kansas Agricultural Experiment Station (C.T.).

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Authors

Contributions

M.W.H., M.N., J.O.B. and J.B. conceived of and designed the experiments. M.W.H., A.M.H. and C.T. carried out all population genetic analyses. A.A. developed the method used to identify hotspots of recombination. S.A., N.W.M. and A.P. were responsible for the experimental aspects of choosing and genotyping the selected lines. Y.S.H. and B.J.V. analyzed the raw array data. F.G.S. designed the maps shown in the manuscript and on the project website. M.W.H. and J.B. wrote the paper. All other authors commented on the manuscript.

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Correspondence to Joy Bergelson.

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The authors declare no competing financial interests.

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Supplementary Figures 1–5, Supplementary Tables 1 and 2 and Supplementary Note. (PDF 455 kb)

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Horton, M., Hancock, A., Huang, Y. et al. Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat Genet 44, 212–216 (2012). https://doi.org/10.1038/ng.1042

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