Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

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

Nature Plants volume 1, Article number: 14023 (2015) Cite this article

Subjects

Abstract

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

References

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  11. Tedder, A., Ansell, S. W., Lao, X., Vogel, J. C. & Mable, B. K. Sporophytic self-incompatibility genes and mating system variation in Arabis alpina. Ann. Bot. 108, 699–713 (2011).

    Article  CAS  Google Scholar 

  12. Wingler, A., Stangberg, E. J., Saxena, T. & Mistry, R. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Hollister, J. D., Smith, L. M., Guo, Y-L., Ott, F., Weigel, D. & Gaut, B. S. 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).

    Article  CAS  Google Scholar 

  20. Hall, A. E., Kettler, G. C. & Preuss, D. Dynamic evolution at pericentromeres. Genome Res. 16, 355–364 (2006).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  22. 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 

  23. Zhang, X., Bernatavichute, Y. V., Cokus, S., Pellegrini, M. & Jacobsen, S. E. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, R62 (2009).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  26. Law, J. A. & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev. Genet. 11, 204–220 (2010).

    Article  CAS  Google Scholar 

  27. Zemach, A., McDaniel, I. E., Silva, P. & Zilberman, D. Genome-wide evolutionary analysis of eukaryotic DNA Methylation. Science 328, 916–919 (2010).

    Article  CAS  Google Scholar 

  28. Matzke, M., Kanno, T., Daxinger, L., Huettel, B. & Matzke, A. J. M. RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21, 367–376 (2009).

    Article  CAS  Google Scholar 

  29. Tsukahara, S., Kobayashi, A., Kawabe, A., Mathieu, O., Miura, A. & Kakutani, T. Bursts of retrotransposition reproduced in Arabidopsis. Nature 461, 423–426 (2009).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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

  1. Geo Velikkakam James

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

  2. Karl J.V. Nordström

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

  3. Claudia Chica

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

  4. Bogna Szarzynska

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

  5. Matthias Zytnicki

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

  6. Maria C. Albani

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

  7. Sara Bergonzi

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

  8. Loren Castaings

    Present address: ‡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.),

  9. Julieta L. Mateos

    Present address: ‡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.);,

  10. Nora Bujdoso

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

  11. Laura de Lorenzo

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

  12. Cristina Barrero-Sicilia

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

  13. Isabel Mateos

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

  14. Romy Chen-Min-Tao

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

  15. Seth J. Davis

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

  16. Eva-Maria Willing, Vimal Rawat and Terezie Mandáková: These authors contributed equally to this work

Authors and Affiliations

  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, 78026, Versailles, 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, 0200, ACT, 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, 16802, Pennsylvania, USA

    Stephan C. Schuster

Authors
  1. Eva-Maria Willing
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vimal Rawat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Terezie Mandáková
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florian Maumus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Geo Velikkakam James
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Karl J.V. Nordström
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Claude Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Norman Warthmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudia Chica
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bogna Szarzynska
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Matthias Zytnicki
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Maria C. Albani
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Christiane Kiefer
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Sara Bergonzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Loren Castaings
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Julieta L. Mateos
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Markus C. Berns
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Nora Bujdoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Thomas Piofczyk
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Laura de Lorenzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Cristina Barrero-Sicilia
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Isabel Mateos
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Mathieu Piednoël
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Jörg Hagmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Romy Chen-Min-Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Raquel Iglesias-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Stephan C. Schuster
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Carlos Alonso-Blanco
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. François Roudier
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Pilar Carbonero
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Javier Paz-Ares
    View author publications

    You can also search for this author in PubMed Google Scholar

  32. Seth J. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  33. Ales Pecinka
    View author publications

    You can also search for this author in PubMed Google Scholar

  34. Hadi Quesneville
    View author publications

    You can also search for this author in PubMed Google Scholar

  35. Vincent Colot
    View author publications

    You can also search for this author in PubMed Google Scholar

  36. Martin A. Lysak
    View author publications

    You can also search for this author in PubMed Google Scholar

  37. Detlef Weigel
    View author publications

    You can also search for this author in PubMed Google Scholar

  38. George Coupland
    View author publications

    You can also search for this author in PubMed Google Scholar

  39. Korbinian Schneeberger
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding authors

Correspondence to George Coupland or Korbinian Schneeberger.

Ethics declarations

Competing interests

The authors declare that no competing interests exist.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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). https://doi.org/10.1038/nplants.2014.23

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2014.23

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing