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.

  • Subscribe to Nature Plants for full access:



Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.


  1. 1.

    The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).

  2. 2.

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

  3. 3.

    et al. The genome of the mesopolyploid crop species Brassica rapa. Nature Genet 43, 1035–1039 (2011).

  4. 4.

    et al. The genome of the extremophile crucifer Thellungiella parvula. Nature Genet. 43, 913–918 (2011).

  5. 5.

    et al. Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc. Natl Acad. Sci. USA 109, 12219–12224 (2012).

  6. 6.

    et al. The reference genome of the halophytic plant Eutrema salsugineum. Front. Plant Sci. 4, 46 (2013).

  7. 7.

    et al. The Tarenaya hassleriana genome provides insight into reproductive trait and genome evolution of crucifers. Plant Cell 25, 2813–2830 (2013).

  8. 8.

    et al. An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nature Genet. 45, 891–898 (2013).

  9. 9.

    et al. The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nature Genet. 45, 831–835 (2013).

  10. 10.

    et al. The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nature Commun. 5, 3930 (2014).

  11. 11.

    , , , & Sporophytic self-incompatibility genes and mating system variation in Arabis alpina. Ann. Bot. 108, 699–713 (2011).

  12. 12.

    , , & Interactions between temperature and sugars in the regulation of leaf senescence in the perennial herb Arabis alpina L. J. Integr. Plant Biol. 54, 595–605 (2012).

  13. 13.

    et al. PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423–427 (2009).

  14. 14.

    & Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann. Bot. 82, 37–44 (1998).

  15. 15.

    & Ancestral repeats have shaped epigenome and genome composition for millions of years in Arabidopsis thaliana. Nature Commun. 5, 4104 (2014).

  16. 16.

    & Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl Acad. Sci. USA 101, 12404–12410 (2004).

  17. 17.

    et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126, 1189–1201 (2006).

  18. 18.

    et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928–1938 (2011).

  19. 19.

    , , , , & Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc. Natl Acad. Sci. USA 108, 2322–2327 (2011).

  20. 20.

    , & Dynamic evolution at pericentromeres. Genome Res. 16, 355–364 (2006).

  21. 21.

    et al. The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. eLife 2, e01426 (2013).

  22. 22.

    et al. Comparing the linkage maps of the close relatives Arabidopsis lyrata and A. thaliana. Genetics 168, 1575–1584 (2004).

  23. 23.

    , , , & Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, R62 (2009).

  24. 24.

    et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219 (2008).

  25. 25.

    et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480, 245–249 (2011).

  26. 26.

    & Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev. Genet. 11, 204–220 (2010).

  27. 27.

    , , & Genome-wide evolutionary analysis of eukaryotic DNA Methylation. Science 328, 916–919 (2010).

  28. 28.

    , , , & RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21, 367–376 (2009).

  29. 29.

    , , , , & Bursts of retrotransposition reproduced in Arabidopsis. Nature 461, 423–426 (2009).

  30. 30.

    et al. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461, 427–430 (2009).

Download references


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.

Author information

Author notes

    • Eva-Maria Willing
    • , Vimal Rawat
    •  & Terezie Mandáková

    These authors contributed equally to this work

    • Geo Velikkakam James

    Present address: Rijk Zwaan R&D Fijnaart, Fijnaart, The Netherlands (G.V.J.)

    • Karl J.V. Nordström

    Present address: Laboratory of EpiGenetics, University of Saarland, Saarbrücken, Germany (K.J.V.N.)

    • Claudia Chica

    Present address: Departamento de Ciencias Biológicas, Universidad de los Andes, Carrera 1 N° 18A- 12, Bogotá, Colombia (C.C.)

    • Bogna Szarzynska

    Present address: Center for Integrative Genomics, University of Lausanne, Genopode Building, CH-1015 Lausanne, Switzerland (B.S-E.)

    • Matthias Zytnicki

    Present address: INRA, MIAT UR-875, Castanet-Tolosan 31320, France (M.Z.)

    • Maria C. Albani

    Present address: Botanical Institute, University of Cologne, Zülpicher Strasse 47B, D-50674 Cologne, Germany (M.C.A.)

    • Sara Bergonzi

    Present address: Laboratory of Plant Breeding, Department of Plant Sciences, Wageningen-UR, PO Box 386, 6700 Wageningen AJ, The Netherlands (S.B.)

    • Loren Castaings

    Present address: Biochimie et Physiologie Moléculaire des Plantes, Centre National de la Recherche Scientifique Unité Mixte de Recherche 5004, Institut de Biologie Intégrative des Plantes, 2 place Pierre Viala, F-34060 Montpellier Cedex 2, France (L.C.)

    • Julieta L. Mateos

    Present address: Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas de Buenos Aires-Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina, C1405BWE Buenos Aires, Argentina (J.M.);

    • Nora Bujdoso

    Present address: Department for Training CUR-BIL-BAN-ELB, Currenta GmbH & Co. OHG, Aprather Weg 18a, 42096 Wuppertal, Germany (N.B.);

    • Laura de Lorenzo

    Present address: Department Plant & Soil Sciences, University of Kentucky, 301C Plant Science Building, 1405 Veterans Drive, Lexington, Kentucky 40546-0312, USA (L.d.L.);

    • Cristina Barrero-Sicilia

    Present address: Biological Chemistry and Crop Protection Department, Rothamsted Research, Harpenden AL5 2JQ, UK (C.B-S.);

    • Isabel Mateos

    Present address: Centro Hispano-Luso de Investigaciones Agrarias-CIALE, Salamanca, Spain (I.M.);

    • Romy Chen-Min-Tao

    Present address: Plateforme Bioinformatique, Institut Gustave Roussy, 94805 Villejuif, France (R.C-M-T.);

    • Seth J. Davis

    Present address: Department of Biology, University of York, York, UK (S.J.D.).


  1. Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, Carl-von-Linné Weg 10, D-50829 Cologne, Germany

    • Eva-Maria Willing
    • , Vimal Rawat
    • , Geo Velikkakam James
    • , Karl J.V. Nordström
    • , Maria C. Albani
    • , Christiane Kiefer
    • , Sara Bergonzi
    • , Loren Castaings
    • , Julieta L. Mateos
    • , Markus C. Berns
    • , Nora Bujdoso
    • , Thomas Piofczyk
    • , Mathieu Piednoël
    • , Seth J. Davis
    • , Ales Pecinka
    • , George Coupland
    •  & Korbinian Schneeberger
  2. Research group Plant Cytogenomics, CEITEC – Central European Institute of Technology, Masaryk University, Brno, Czech Republic

    • Terezie Mandáková
    •  & Martin A. Lysak
  3. INRA, UR1164 URGI—Research Unit in Genomics-Info, INRA de Versailles-Grignon, Route de Saint-Cyr, Versailles 78026, France

    • Florian Maumus
    • , Matthias Zytnicki
    •  & Hadi Quesneville
  4. Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany

    • Claude Becker
    • , Norman Warthmann
    • , Jörg Hagmann
    •  & Detlef Weigel
  5. Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia

    • Norman Warthmann
  6. Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) UMR 8197 and Institut National de la Santé et de la Recherche Médicale (INSERM) U 1024, Paris, France

    • Claudia Chica
    • , Bogna Szarzynska
    • , Romy Chen-Min-Tao
    • , François Roudier
    •  & Vincent Colot
  7. Department of Plant Molecular Genetics, Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas (CSIC), Campus de Cantoblanco, 28049 Madrid, Spain

    • Laura de Lorenzo
    • , Isabel Mateos
    • , Carlos Alonso-Blanco
    •  & Javier Paz-Ares
  8. Centro de Biotecnología y Genómica de Plantas (UPM-INIA). ETSI agrónomos, Universidad Politécnica de Madrid, Campus de Montegancedo, Pozuelo de Alarcón, 28223 Madrid, Spain

    • Cristina Barrero-Sicilia
    • , Raquel Iglesias-Fernández
    •  & Pilar Carbonero
  9. Center for Comparative Genomics and Bioinformatics, Pennsylvania State University, University Park, Pennsylvania 16802, USA

    • Stephan C. Schuster


  1. Search for Eva-Maria Willing in:

  2. Search for Vimal Rawat in:

  3. Search for Terezie Mandáková in:

  4. Search for Florian Maumus in:

  5. Search for Geo Velikkakam James in:

  6. Search for Karl J.V. Nordström in:

  7. Search for Claude Becker in:

  8. Search for Norman Warthmann in:

  9. Search for Claudia Chica in:

  10. Search for Bogna Szarzynska in:

  11. Search for Matthias Zytnicki in:

  12. Search for Maria C. Albani in:

  13. Search for Christiane Kiefer in:

  14. Search for Sara Bergonzi in:

  15. Search for Loren Castaings in:

  16. Search for Julieta L. Mateos in:

  17. Search for Markus C. Berns in:

  18. Search for Nora Bujdoso in:

  19. Search for Thomas Piofczyk in:

  20. Search for Laura de Lorenzo in:

  21. Search for Cristina Barrero-Sicilia in:

  22. Search for Isabel Mateos in:

  23. Search for Mathieu Piednoël in:

  24. Search for Jörg Hagmann in:

  25. Search for Romy Chen-Min-Tao in:

  26. Search for Raquel Iglesias-Fernández in:

  27. Search for Stephan C. Schuster in:

  28. Search for Carlos Alonso-Blanco in:

  29. Search for François Roudier in:

  30. Search for Pilar Carbonero in:

  31. Search for Javier Paz-Ares in:

  32. Search for Seth J. Davis in:

  33. Search for Ales Pecinka in:

  34. Search for Hadi Quesneville in:

  35. Search for Vincent Colot in:

  36. Search for Martin A. Lysak in:

  37. Search for Detlef Weigel in:

  38. Search for George Coupland in:

  39. Search for Korbinian Schneeberger in:


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.

Competing interests

The authors declare that no competing interests exist.

Corresponding authors

Correspondence to George Coupland or Korbinian Schneeberger.

Supplementary information

About this article

Publication history






Rights and permissions

To obtain permission to re-use content from this article visit RightsLink.