The Arabidopsis lyrata genome sequence and the basis of rapid genome size change (original) (raw)

References

1. Greilhuber, J. et al. Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size. Plant Biol. 8, 770–777 (2006).
   Article CAS Google Scholar
2. Gregory, T.R. et al. Eukaryotic genome size databases. Nucleic Acids Res. 35, D332–D338 (2007).
   Article CAS Google Scholar
3. Gaut, B.S. & Ross-Ibarra, J. Selection on major components of angiosperm genomes. Science 320, 484–486 (2008).
   Article CAS Google Scholar
4. Pellicer, J., Fay, M.F. & Leitch, I.J. The largest eukaryotic genome of them all? Bot. J. Linn. Soc. 164, 10–15 (2010).
   Article Google Scholar
5. Bennetzen, J.L., Ma, J. & Devos, K.M. Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95, 127–132 (2005).
   Article CAS Google Scholar
6. Hawkins, J.S., Proulx, S.R., Rapp, R.A. & Wendel, J.F. Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc. Natl. Acad. Sci. USA 106, 17811–17816 (2009).
   Article CAS Google Scholar
7. Piegu, B. et al. Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 16, 1262–1269 (2006).
   Article CAS Google Scholar
8. Vitte, C., Panaud, O. & Quesneville, H. LTR retrotransposons in rice (Oryza sativa, L.): recent burst amplifications followed by rapid DNA loss. BMC Genomics 8, 218 (2007).
   Article Google Scholar
9. Woodhouse, M.R. et al. Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homologs. PLoS Biol. 8, e1000409 (2010).
   Article Google Scholar
10. Paterson, A.H. et al. The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551–556 (2009).
    Article CAS Google Scholar
11. Johnston, J.S. et al. Evolution of genome size in Brassicaceae. Ann. Bot. 95, 229–235 (2005).
    Article CAS Google Scholar
12. Oyama, R.K. et al. The shrunken genome of Arabidopsis thaliana. Plant Syst. Evol. 273, 257–271 (2008).
    Article CAS Google Scholar
13. Wright, S.I., Lauga, B. & Charlesworth, D. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19, 1407–1420 (2002).
    Article CAS Google Scholar
14. Ossowski, S. et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92–94 (2010).
    Article CAS Google Scholar
15. Beilstein, M.A., Nagalingum, N.S., Clements, M.D., Manchester, S.R. & Mathews, S. Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 107, 18724–18728 (2010).
    Article CAS Google Scholar
16. Kuittinen, H. et al. Comparing the linkage maps of the close relatives Arabidopsis lyrata and A. thaliana. Genetics 168, 1575–1584 (2004).
    Article CAS Google Scholar
17. Koch, M.A. & Kiefer, M. Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diplod species–—Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana. Am. J. Bot. 92, 761–767 (2005).
    Article Google Scholar
18. Yogeeswaran, K. et al. Comparative genome analyses of Arabidopsis spp.: inferring chromosomal rearrangement events in the evolutionary history of A. thaliana. Genome Res. 15, 505–515 (2005).
    Article CAS Google Scholar
19. Lysak, M.A. et al. Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc. Natl. Acad. Sci. USA 103, 5224–5229 (2006).
    Article CAS Google Scholar
20. Berr, A. et al. Chromosome arrangement and nuclear architecture but not centromeric sequences are conserved between Arabidopsis thaliana and Arabidopsis lyrata. Plant J. 48, 771–783 (2006).
    Article CAS Google Scholar
21. Swarbreck, D. et al. The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res. 36, D1009–10014 (2007).
    Article Google Scholar
22. Lim, J.K. & Simmons, M.J. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays 16, 269–275 (1994).
    Article CAS Google Scholar
23. Stankiewicz, P. et al. Genome architecture catalyzes nonrecurrent chromosomal rearrangements. Am. J. Hum. Genet. 72, 1101–1116 (2003).
    Article CAS Google Scholar
24. Korbel, J.O. et al. Paired-end mapping reveals extensive structural variation in the human genome. Science 318, 420–426 (2007).
    Article CAS Google Scholar
25. Lee, J., Han, K., Meyer, T.J., Kim, H.S. & Batzer, M.A. Chromosomal inversions between human and chimpanzee lineages caused by retrotransposons. PLoS ONE 3, e4047 (2008).
    Article Google Scholar
26. Braumann, I., van den Berg, M.A. & Kempken, F. Strain-specific retrotransposon-mediated recombination in commercially used Aspergillus niger strain. Mol. Genet. Genomics 280, 319–325 (2008).
    Article CAS Google Scholar
27. Woodhouse, M.R., Pedersen, B. & Freeling, M. Transposed genes in Arabidopsis are often associated with flanking repeats. PLoS Genet. 6, e1000949 (2010).
    Article Google Scholar
28. Ranz, J.M. et al. Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biol. 5, e152 (2007).
    Article Google Scholar
29. The Chimpanzee Sequencing and Analysis Consortium. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437, 69–87 (2005).
30. Clark, R.M. et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338–342 (2007).
    Article CAS Google Scholar
31. Borevitz, J.O. et al. Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104, 12057–12062 (2007).
    Article CAS Google Scholar
32. Enright, A.J., Van Dongen, S. & Ouzounis, C.A. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30, 1575–1584 (2002).
    Article CAS Google Scholar
33. Michelmore, R.W. & Meyers, B.C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8, 1113–1130 (1998).
    Article CAS Google Scholar
34. Thomas, J.H. Adaptive evolution in two large families of ubiquitin-ligase adapters in nematodes and plants. Genome Res. 16, 1017–1030 (2006).
    Article CAS Google Scholar
35. Yang, X. et al. The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol. 148, 1189–1200 (2008).
    Article CAS Google Scholar
36. Tuskan, G.A. et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596–1604 (2006).
    Article CAS Google Scholar
37. Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463–467 (2007).
    Article CAS Google Scholar
38. Velasco, R. et al. A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2, e1326 (2007).
    Article Google Scholar
39. Li, L., Stoeckert, C.J. Jr. & Roos, D.S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–2189 (2003).
    Article CAS Google Scholar
40. 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
41. Devos, K.M., Brown, J.K. & Bennetzen, J.L. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 12, 1075–1079 (2002).
    Article CAS Google Scholar
42. Hollister, J.D. & Gaut, B.S. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 19, 1419–1428 (2009).
    Article CAS Google Scholar
43. Nordborg, M. et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196 (2005).
    Article Google Scholar
44. Petrov, D.A., Sangster, T.A., Johnston, J.S., Hartl, D.L. & Shaw, K.L. Evidence for DNA loss as a determinant of genome size. Science 287, 1060–1062 (2000).
    Article CAS Google Scholar
45. Petrov, D.A., Lozovskaya, E.R. & Hartl, D.L. High intrinsic rate of DNA loss in Drosophila. Nature 384, 346–349 (1996).
    Article CAS Google Scholar
46. Charlesworth, B. Evolutionary rates in partially self-fertilizing species. Am. Nat. 140, 126–148 (1992).
    Article CAS Google Scholar
47. Knight, C.A., Molinari, N.A. & Petrov, D.A. The large genome constraint hypothesis: evolution, ecology and phenotype. Ann. Bot. 95, 177–190 (2005).
    Article CAS Google Scholar
48. Jaffe, D.B. et al. Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res. 13, 91–96 (2003).
    Article CAS Google Scholar
49. Demuth, J.P., De Bie, T., Stajich, J.E., Cristianini, N. & Hahn, M.W. The evolution of mammalian gene families. PLoS ONE 1, e85 (2006).
    Article Google Scholar
50. Prachumwat, A. & Li, W.H. Gene number expansion and contraction in vertebrate genomes with respect to invertebrate genomes. Genome Res. 18, 221–232 (2008).
    Article CAS Google Scholar
51. Drosophila 12 Genomes Consortium. et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450, 203–218 (2007).
52. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. The CLUSTAL-X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882 (1997).
    Article CAS Google Scholar
53. Wicker, T. et al. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973–982 (2007).
    Article CAS Google Scholar
54. McCarthy, E.M. & McDonald, J.F. LTR_STRUC: a novel search and identification program for LTR retrotransposons. Bioinformatics 19, 362–367 (2003).
    Article CAS Google Scholar
55. Edgar, R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004).
    Article Google Scholar
56. Xiong, Y. & Eickbush, T.H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9, 3353–3362 (1990).
    Article CAS Google Scholar
57. Zhang, X. & Wessler, S.R. Genome-wide comparative analysis of the transposable elements in the related species Arabidopsis thaliana and Brassica oleracea. Proc. Natl. Acad. Sci. USA 101, 5589–5594 (2004).
    Article CAS Google Scholar
58. Swofford, D.L. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods): Version 4. (Sinauer Associates, Sunderland, Massachusetts, USA, 2003).
59. Simillion, C., Vandepoele, K., Saeys, Y. & Van de Peer, Y. Building genomic profiles for uncovering segmental homology in the twilight zone. Genome Res. 14, 1095–1106 (2004).
    Article CAS Google Scholar
60. Altschul, S.F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).
    Article CAS Google Scholar
61. Smith, T.F. & Waterman, M.S. Identification of common molecular subsequences. J. Mol. Biol. 147, 195–197 (1981).
    Article CAS Google Scholar
62. Pearson, W.R. Searching protein sequence libraries: comparison of the sensitivity and selectivity of the Smith-Waterman and FASTA algorithms. Genomics 11, 635–650 (1991).
    Article CAS Google Scholar
63. Kent, W.J. BLAT–—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002).
    Article CAS Google Scholar
64. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
    Article CAS Google Scholar
65. Katoh, K., Asimenos, G. & Toh, H. Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537, 39–64 (2009).
    Article CAS Google Scholar

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Acknowledgements

The US Department of Energy Joint Genome Institute (JGI) provided sequencing and analyses under the Community Sequencing Program supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. We are particularly grateful to D. Rokhsar and K. Barry for providing leadership for the project at JGI. We thank J. Borevitz, A. Hall, C. Langley, J. Nasrallah, B. Neuffer, O. Savolainen and S. Wright for contributing to the initial sequencing proposal submitted to the Community Sequencing Program at JGI, C. Lanz and K. Lett for technical assistance, and P. Andolfatto and R. Wing for comments on the manuscript. This work was supported by National Science Foundation (NSF) DEB-0723860 (B.S.G.), NSF DEB-0723935 (M.N.), NSF MCB-0618433 (J.C.C.), NSF IOS-0744579 (M.E.N.), NIH GM057994 (J.B.), grant GABI-DUPLO 0315055 of the German Federal Ministry of Education and Research (K.F.X.M.), ERA-NET on Plant Genomics (ERA-PG) grant ARelatives from the Deutsche Forschungsgemeinschaft (D.W.) and Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT) and the Inter-University Network for Fundamental Research (P6/25, BioMaGNet) (Y.V.d.P.), a Gottfried Wilhelm Leibniz Award of Deutsche Forschungsgemeinschaft (DFG) (D.W.), the Austria Academy of Sciences (M.N.) and the Max Planck Society (D.W. and Y.-L.G.).

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Author notes

1. Tina T Hu, Erica G Bakker, Richard M Clark, Jeffrey A Fawcett, Jesse D Hollister, Stephan Ossowski, Korbinian Schneeberger & Xi Wang
   Present address: Present addresses: Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey 08544, USA (T.T.H.), Dow AgroSciences, Portland, Oregon 97224, USA (E.G.B.), Department of Biology, University of Utah, Salt Lake City, Utah, USA (R.M.C.), Graduate University for Advanced Studies, Hayama, Kanagawa, Japan (J.A.F.), Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA (J.D.H.), Center for Genomic Regulation, Barcelona, Spain (S.O.), Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany (K.S.) and Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany (X.W.).,
2. Tina T Hu and Pedro Pattyn: These authors contributed equally to this work.

Authors and Affiliations

1. Molecular and Computational Biology, University of Southern California, Los Angeles, California, USA
   Tina T Hu & Magnus Nordborg
2. Department of Plant Systems Biology, VIB, Gent, Belgium
   Pedro Pattyn, Jeffrey A Fawcett & Yves Van de Peer
3. Department of Plant Biotechnology and Genetics, Ghent University, Gent, Belgium
   Pedro Pattyn, Jeffrey A Fawcett & Yves Van de Peer
4. Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, USA
   Erica G Bakker & Joy Bergelson
5. Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, USA
   Erica G Bakker, Noah Fahlgren & James C Carrington
6. Department of Horticulture, Oregon State University, Corvallis, Oregon, USA
   Erica G Bakker
7. Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
   Jun Cao, Richard M Clark, Stephan Ossowski, Korbinian Schneeberger, Detlef Weigel & Ya-Long Guo
8. US Department of Energy Joint Genome Institute, Walnut Creek, California, USA
   Jan-Fang Cheng, Jane Grimwood, Robert P Ottilar, Asaf A Salamov, Jeremy Schmutz & Igor V Grigoriev
9. Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA
   Noah Fahlgren & James C Carrington
10. HudsonAlpha Genome Sequencing Center, HudsonAlpha Institute for Biotechnology, Huntsville, Alabama, USA
    Jane Grimwood & Jeremy Schmutz
11. Munich Information Center for Protein Sequences/Institute for Bioinformatics and Systems Biology, Helmholtz Center Munich, Neuherberg, Germany
    Heidrun Gundlach, Georg Haberer, Manuel Spannagl, Xi Wang & Klaus F X Mayer
12. Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, California, USA
    Jesse D Hollister, Liang Yang & Brandon S Gaut
13. Department of Plant Biology, Cornell University, Ithaca, New York, USA
    Mikhail E Nasrallah
14. Gregor Mendel Institute, Austrian Academy of Science, Vienna, Austria
    Magnus Nordborg

Authors

1. Tina T Hu
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2. Pedro Pattyn
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3. Erica G Bakker
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4. Jun Cao
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5. Jan-Fang Cheng
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6. Richard M Clark
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7. Noah Fahlgren
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8. Jeffrey A Fawcett
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9. Jane Grimwood
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10. Heidrun Gundlach
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11. Georg Haberer
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12. Jesse D Hollister
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13. Stephan Ossowski
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14. Robert P Ottilar
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15. Asaf A Salamov
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16. Korbinian Schneeberger
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17. Manuel Spannagl
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18. Xi Wang
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19. Liang Yang
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20. Mikhail E Nasrallah
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21. Joy Bergelson
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22. James C Carrington
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23. Brandon S Gaut
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24. Jeremy Schmutz
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25. Klaus F X Mayer
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26. Yves Van de Peer
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27. Igor V Grigoriev
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28. Magnus Nordborg
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29. Detlef Weigel
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30. Ya-Long Guo
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Contributions

J.B., J.C.C., B.S.G., I.V.G., Y.-L.G., K.F.X.M., M.N., Y.V.d.P. and D.W. conceived the study; M.E.N. provided the biological material; J.C., J.-F.C., R.M.C., N.F., J.G. and Y.-L.G. performed the experiments; E.G.B., J.A.F., N.F., H.G., Y.-L.G., G.H., J.D.H., T.T.H., R.P.O., S.O., P.P., A.A.S., J.S., K.S., M.S., X.W. and L.Y. analyzed the data; and Y.-L.G., T.T.H., M.N. and D.W. wrote the paper with contributions from all authors.

Corresponding authors

Correspondence toDetlef Weigel or Ya-Long Guo.

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Hu, T., Pattyn, P., Bakker, E. et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change.Nat Genet 43, 476–481 (2011). https://doi.org/10.1038/ng.807

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• Received: 13 September 2010
• Accepted: 18 March 2011
• Published: 10 April 2011
• Issue Date: May 2011
• DOI: https://doi.org/10.1038/ng.807