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Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation


Despite evolutionary conserved mechanisms to silence transposable element activity, there are drastic differences in the abundance of transposable elements even among closely related plant species. We conducted a de novo assembly for the 375 Mb genome of the perennial model plant, Arabis alpina. Analysing this genome revealed long-lasting and recent transposable element activity predominately driven by Gypsy long terminal repeat retrotransposons, which extended the low-recombining pericentromeres and transformed large formerly euchromatic regions into repeat-rich pericentromeric regions. This reduced capacity for long terminal repeat retrotransposon silencing and removal in A. alpina co-occurs with unexpectedly low levels of DNA methylation. Most remarkably, the striking reduction of symmetrical CG and CHG methylation suggests weakened DNA methylation maintenance in A. alpina compared with Arabidopsis thaliana. Phylogenetic analyses indicate a highly dynamic evolution of some components of methylation maintenance machinery that might be related to the unique methylation in A. alpina.

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Figure 1: Phylogenetic reconstruction and karyotype evolution support a distinct phylogenetic placement of A. alpina.
Figure 2: Genome size variation and differences in transposable element content.
Figure 3: Differences in the distribution of genes, transposable elements and chromatin marks between A. thaliana, A. lyrata and A. alpina.
Figure 4: Species-specific differences in DNA methylation.


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We thank José Jiménez-Gómez for helpful discussion throughout the entire project and Marcus Koch, Maarten Koornneef as well as Miltos Tsiantis for critical reading of the manuscript. We apologize to all colleagues whose work has not been cited here because of space constraints. The TRANSNET consortium was initiated based on the funding of PLANT KBBE ‘Transcriptional networks and their evolution in the Brassicaceae (TRANSNET)’. B.S. was supported by a postdoctoral fellowship from the TRANSNET consortium. C.C. was supported by a postdoctoral fellowship first from Investissements d'Avenir ANR-10-LABX-54 MEMO LIFE and then from the European Union EpiGeneSys FP7 Network of Excellence (number 257082). R.C.M.T. was supported by Investissements d'Avenir ANR-10-LABX-54 MEMO LIFE. J.L.M was supported by an Alexander von Humboldt Postdoctoral Fellowship. C.B.S was supported by a postdoctoral fellowship from the TRANSNET consortium. R.I.F. was supported by a post-doctoral Juan de la Cierva contract (JCI-2010-07909) from Ministerio de Ciencia e Innovación (MICINN). A.P. was supported by the research grant PE-1853/2 from German Research Foundation. Work in the Carbonero's group was supported by the Spanish grants BFU2009-11809 and Consolider CSD2007-00057 from Ministerio de Ciencia e Innovación (MICINN). C.A-B. laboratory was funded by grant BIO2013-45407-P from the Ministerio de Economía y Competitividad of Spain. Work in the Colot group was supported by the Agence Nationale de la Recherche (Investissements d'Avenir ANR-10-LABX-54 MEMO LIFE and ANR-11-IDEX-0001-02 PSL* Research University) and the European Union (EpiGeneSys FP7 Network of Excellence number 257082). Work in the Weigel group was supported by an FP7 project AENEAS and the TRANSNET consortium. Work in the Quesneville group was supported by the TRANSNET consortium and by the French national research agency (ANR-08-KBBE-012). Work in the Lysak group was supported by a research grant from the Czech Science Foundation (P501/12/G090) and by the European Social Fund (projects CZ.1.07/2.3.00/30.0037 and CZ.1.07/2.3.00/20.0189). Work on A. alpina in the Coupland laboratory is partly funded by the Cluster of Excellence on Plant Sciences (CEPLAS). Work in the Paz-Ares laboratory has been supported by the French-German-Spanish Trilateral program on Plant Genomics (grant TRANSNET) and Spanish Ministry of Economy competiveness (CONSOLIDER 2007-28317, BIO2011-30546). Schneeberger, Coupland, Weigel and Pecinka groups were supported by the Max Planck Society.

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E.M.W., S.C.S., C.A-B., F.R., P.C., J.P.A., S.J.D., A.P., H.Q., V.C., M.A.L., D.W., G.C. and K.S. conceived this study and supervised experiments and analyses. L.C., M.C.A., B.S., S.B., L.C., J.L.M., M.C.B., N.B., T.P., L.D.L., I.M. and C.B.S. prepared samples for DNA and RNA sequencing. B.S. prepared samples and performed ChIP and MeDIP experiments. C.B. prepared samples and performed bisulphite experiments. N.W., M.C.A. and C.A-B. constructed genetic maps. T.M. and M.A.L. conducted FISH, chromosome painting and karyotype evolution analysis. K.J.V.N., E.M.W. and N.W. conducted de novo assembly of A. alpina. C.K. conducted de novo assembly of A. montbretiana. G.V.J., E.M.W., C.B.S. and M.Z. performed genome annotations of A. alpina together with all participants of the annotation jamboree held in 2012 in Paris, France. E.M.W. performed genome annotations of A. montbretiana. E.M.W., V.R. and C.C. conducted expression analyses. F.M. performed transposon annotations. E.M.W., F.M., M.P. and K.S. performed transposon analysis. E.M.W., C.C., R.C.M.T. and K.S. performed analysis of ChIP-seq and MeDIP-seq data. E.M.W., C.B., J.H. and K.S. performed BS-seq analysis. E.M.W., V.R. and K.S. conducted comparative genomic analyses. E.M.W. and K.S. wrote the paper with contributions from all authors.

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Correspondence to George Coupland or Korbinian Schneeberger.

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Willing, EM., Rawat, V., Mandáková, T. et al. Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nature Plants 1, 14023 (2015).

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