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.

  • Letter
  • Published:

Selective epigenetic control of retrotransposition in Arabidopsis

Nature volume 461, pages 427–430 (2009)Cite this article

Abstract

Retrotransposons are mobile genetic elements that populate chromosomes, where the host largely controls their activities1,2,3. In plants and mammals, retrotransposons are transcriptionally silenced by DNA methylation1,4, which in Arabidopsis is propagated at CG dinucleotides by METHYLTRANSFERASE 1 (MET1)5. In met1 mutants, however, mobilization of retrotransposons is not observed, despite their transcriptional activation4,5,6. A post-transcriptional mechanism therefore seems to be preventing retrotransposition. Here we show that a copia-type retrotransposon (Évadé, French for ‘fugitive’) evaded suppression of its movement during inbreeding of hybrid epigenomes consisting of met1- and wild-type-derived chromosomes. Évadé (EVD) reinsertions caused a series of developmental mutations that allowed its identification. Genetic testing of host control of the EVD life cycle showed that transcriptional suppression occurred by CG methylation supported by RNA-directed DNA methylation. On transcriptional reactivation, subsequent steps of the EVD cycle were inhibited by plant-specific RNA polymerase IV/V7,8 and the histone methyltransferase KRYPTONITE (KYP). Moreover, genome resequencing demonstrated retrotransposition of EVD but no other potentially active retroelements when this combination of epigenetic mechanisms was compromised. Our results demonstrate that epigenetic control of retrotransposons extends beyond transcriptional suppression and can be individualized for particular elements.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Mobilization of EVD LTR retrotransposon in epiRILs.
Figure 2: EVD life cycle in epiRILs and the met1-3 parent.
Figure 3: Genetic analysis of EVD transposition control.

Similar content being viewed by others

References

  1. Slotkin, R. K. & Martienssen, R. A. Transposable elements and the epigenetic regulation of the genome. Nature Rev. Genet. 8, 272–285 (2007)

    Article  CAS  Google Scholar 

  2. Beauregard, A., Curcio, M. J. & Belfort, M. The take and give between retrotransposable elements and their hosts. Annu. Rev. Genet. 42, 587–617 (2008)

    Article  CAS  Google Scholar 

  3. Goodier, J. L. & Kazazian, H. H. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135, 23–35 (2008)

    Article  CAS  Google Scholar 

  4. 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 

  5. Saze, H., Mittelsten Scheid, O. & Paszkowski, J. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nature Genet. 34, 65–69 (2003)

    Article  CAS  Google Scholar 

  6. Lister, R. et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis . Cell 133, 523–536 (2008)

    Article  CAS  Google Scholar 

  7. Pontier, D. et al. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis . Genes Dev. 19, 2030–2040 (2005)

    Article  CAS  Google Scholar 

  8. Wierzbicki, A. T., Haag, J. R. & Pikaard, C. S. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135, 635–648 (2008)

    Article  CAS  Google Scholar 

  9. Reinders, J. et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23, 939–950 (2009)

    Article  CAS  Google Scholar 

  10. Hirochika, H., Okamoto, H. & Kakutani, T. Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12, 357–369 (2000)

    Article  CAS  Google Scholar 

  11. Matzke, M. A., Kanno, T., Huettel, B., Daxinger, L. & Matzke, A. J. Targets of RNA-directed DNA methylation. Curr. Opin. Plant Biol. 10, 512–519 (2007)

    Article  CAS  Google Scholar 

  12. Brodersen, P. et al. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185–1190 (2008)

    Article  ADS  CAS  Google Scholar 

  13. Slotkin, R. K. et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461–472 (2009)

    Article  CAS  Google Scholar 

  14. Mathieu, O., Reinders, J., Caikovski, M., Smathajitt, C. & Paszkowski, J. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130, 851–862 (2007)

    Article  CAS  Google Scholar 

  15. Jackson, J. P. et al. Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana . Chromosoma 112, 308–315 (2004)

    Article  CAS  Google Scholar 

  16. Ding, Y. et al. SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19, 9–22 (2007)

    Article  CAS  Google Scholar 

  17. Chuikov, S. et al. Regulation of p53 activity through lysine methylation. Nature 432, 353–360 (2004)

    Article  ADS  CAS  Google Scholar 

  18. Kouskouti, A., Scheer, E., Staub, A., Tora, L. & Talianidis, I. Gene-specific modulation of TAF10 function by SET9-mediated methylation. Mol. Cell 14, 175–182 (2004)

    Article  CAS  Google Scholar 

  19. Sampath, S. C. et al. Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly. Mol. Cell 27, 596–608 (2007)

    Article  CAS  Google Scholar 

  20. Jackson, J. P., Lindroth, A., Cao, X. & Jacobsen, S. E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556–560 (2002)

    Article  ADS  CAS  Google Scholar 

  21. Cao, X. et al. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13, 2212–2217 (2003)

    Article  CAS  Google Scholar 

  22. Zhang, X. & Jacobsen, S. E. Genetic analyses of DNA methyltransferases in Arabidopsis thaliana . Cold Spring Harb. Symp. Quant. Biol. 71, 439–447 (2006)

    Article  CAS  Google Scholar 

  23. Miura, A. et al. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis . Nature 411, 212–214 (2001)

    Article  ADS  CAS  Google Scholar 

  24. Tsukahara, S. et al. Burst of retrotransposition reproduced in Arabidopsis . Nature 10.1038/nature08351 (this issue)

  25. Mathieu, O., Probst, A. & Paszkowski, J. Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis . EMBO J. 24, 2783–2791 (2005)

    Article  CAS  Google Scholar 

  26. Chan, S. W. et al. RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis . PLoS Genet. 2, e83 (2006)

    Article  Google Scholar 

  27. Onodera, Y. et al. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120, 613–622 (2005)

    Article  CAS  Google Scholar 

  28. Reinders, J. et al. Genome-wide, high-resolution DNA methylation profiling using bisulfite-mediated cytosine conversion. Genome Res. 18, 469–476 (2008)

    Article  CAS  Google Scholar 

  29. Pall, G. S., Codony-Servat, C., Byrne, J., Ritchie, L. & Hamilton, A. Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res. 35, e60 (2007)

    Article  Google Scholar 

  30. Kanno, T. et al. A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nature Genet. 40, 670–675 (2008)

    Article  CAS  Google Scholar 

  31. Ossowski, S. et al. Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res. 18, 2024–2033 (2008)

    Article  CAS  Google Scholar 

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

Download references

Acknowledgements

We thank all members of the Paszkowski laboratory for discussion; L. Broger, M. Freyre, J. Nicolet, C. Mégies and J. Lafleuriel for technical assistance; M. Dapp and X. Zhang for met1/+ drm1/+ drm2/+ cmt3/+ material; C. Lanz for help in preparing the Illumina libraries and running the instruments and P. King and E. Lacombe for critically reading the manuscript. This work was supported by grants from the Swiss National Science Foundation (3100A0-102107), the European Commission through The Epigenome (LSHG-CT- 2004-503433) and Targeted Gene Integration in Plants (TAGIP; 018785) and the Max Planck Society.

Author Contributions M.M., J.R., J.P. and O.M. conceived the study. M.M., J.R., E.B., T.N. and O.M performed the experiments. K.S., S.O., J.C. and D.W. contributed Illumina sequencing-by-synthesis data and analysis. M.M., J.R., J.P. and O.M. wrote the paper with contributions from all co-authors.

Author information

Author notes

  1. Marie Mirouze and Jon Reinders: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Plant Biology, University of Geneva, Sciences III, 30 Quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland,

    Marie Mirouze, Jon Reinders, Etienne Bucher, Taisuke Nishimura, Jerzy Paszkowski & Olivier Mathieu

  2. Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany

    Korbinian Schneeberger, Stephan Ossowski, Jun Cao & Detlef Weigel

  3. Centre National de la Recherche Scientifique (CNRS), UMR 6247, GReD, INSERM U 931, 24 avenue des Landais, Clermont Université, 63177 Aubière, France

    Olivier Mathieu

Authors
  1. Marie Mirouze
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jon Reinders
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Etienne Bucher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Taisuke Nishimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Korbinian Schneeberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stephan Ossowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jun Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Detlef Weigel
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jerzy Paszkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Olivier Mathieu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jerzy Paszkowski or Olivier Mathieu.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-8 with Legends, Supplementary Table 1 and Supplementary References. (PDF 2847 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mirouze, M., Reinders, J., Bucher, E. et al. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461, 427–430 (2009). https://doi.org/10.1038/nature08328

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature08328

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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