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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.

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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.

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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.

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  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

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  1. Marie Mirouze
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Correspondence to Jerzy Paszkowski or Olivier Mathieu.

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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

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