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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627–631 (2010).
Brachi, B. et al. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet. 6, e1000940 (2010).
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).
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).
Kim, S. et al. Recombination and linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 39, 1151–1155 (2007).
Clark, R.M. et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338–342 (2007).
Patterson, N., Price, A.L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).
Nordborg, M. et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196 (2005).
Platt, A. et al. The scale of population structure in Arabidopsis thaliana. PLoS Genet. 6, e1000843 (2010).
Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43, 956–963 (2011).
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).
McVean, G.A. et al. The fine-scale structure of recombination rate variation in the human genome. Science 304, 581–584 (2004).
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).
Yang, S. et al. Repetitive element–mediated recombination as a mechanism for new gene origination in Drosophila. PLoS Genet. 4, e3 (2008).
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).
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).
Hollister, J.D. & Gaut, B.S. Population and evolutionary dynamics of Helitron transposable elements in Arabidopsis thaliana. Mol. Biol. Evol. 24, 2515–2524 (2007).
Hu, T.T. et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476–481 (2011).
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).
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).
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).
Lichten, M. & Goldman, A.S. Meiotic recombination hotspots. Annu. Rev. Genet. 29, 423–444 (1995).
Morgante, M., Hanafey, M. & Powell, W. Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat. Genet. 30, 194–200 (2002).
Blanc, G. & Wolfe, K.H. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16, 1667–1678 (2004).
Swigonová, Z. et al. Close split of sorghum and maize genome progenitors. Genome Res. 14, 1916–1923 (2004).
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).
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).
Myers, S. et al. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327, 876–879 (2010).
Hancock, A.M. et al. Adaptation to climate across the Arabidopsis thaliana genome. Science 334, 83–86 (2011).
Fournier-Level, A. et al. A map of local adaptation in Arabidopsis thaliana. Science 334, 86–89 (2011).
Smith, J.M. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23–35 (1974).
Toomajian, C. et al. A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biol. 4, e137 (2006).
Nielsen, R. et al. Genomic scans for selective sweeps using SNP data. Genome Res. 15, 1566–1575 (2005).
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).
Hartmann, U. et al. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351–360 (2000).
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).
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).
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).
Lin, X. et al. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402, 761–768 (1999).
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).
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).
Gan, X. et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419–423 (2011).
Anastasio, A.E. et al. Source verification of misidentified Arabidopsis thaliana accessions. Plant J. 67, 554–566 (2011).
Weir, B.S. & Cockerham, C.C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).
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.).
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Text and Figures
Supplementary Figures 1–5, Supplementary Tables 1 and 2 and Supplementary Note. (PDF 455 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng.1042
This article is cited by
-
Molecular mechanisms and regulation of recombination frequency and distribution in plants
Theoretical and Applied Genetics (2024)
-
BGWAS: Bayesian variable selection in linear mixed models with nonlocal priors for genome-wide association studies
BMC Bioinformatics (2023)
-
A VEL3 histone deacetylase complex establishes a maternal epigenetic state controlling progeny seed dormancy
Nature Communications (2023)
-
Single-gene resolution of diversity-driven overyielding in plant genotype mixtures
Nature Communications (2023)
-
Identification of gene function based on models capturing natural variability of Arabidopsis thaliana lipid metabolism
Nature Communications (2023)