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Reconstructing de novo silencing of an active plant retrotransposon

Nature Genetics volume 45, pages 1029–1039 (2013)Cite this article

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Abstract

Transposable elements (TEs) contribute to genome size, organization and evolution. In plants, their activity is primarily controlled by transcriptional gene silencing (TGS), usually investigated at steady states, reflecting how long-established silent conditions are maintained, faithfully reiterated or temporarily modified. How active, invasive TEs are detected and silenced de novo in plants remains largely unknown. Using inbred lineages of hybrid Arabidopsis thaliana epigenomes combining wild-type and mutant chromosomes, we have deciphered the sequence of physiological and molecular events underlying the de novo invasion, proliferation and eventual demise of the single-copy endogenous retrotransposon Evadé (EVD). We show how this reconstructed TE burst causes widespread genome diversification and de novo epiallelism that could serve as sources for selectable and potentially adaptive traits.

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Figure 1: EVD transcript accumulation pattern.
Figure 2: Antiviral PTGS is activated against and suppressed by EVD.
Figure 3: Onset of EVD silencing over multiple generations.
Figure 4: All-or-nothing LTR methylation of EVD copies.
Figure 5: RDR6-DCL3–dependent RdDM triggers EVD TGS.
Figure 6: Genetic and epigenetic consequences of EVD mobilization.
Figure 7: Rise and demise of EVD.

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Acknowledgements

We thank members of the Voinnet laboratory for fruitful discussions and critical reading of the manuscript. C. Brosnan is specially thanked for his intellectual input and support all throughout this project. We are indebted to D. Meyer for help with in situ hybridization. We thank L. Navarro (Institut de Biologie de l'Ecole Nomrale Supérieure, IBENS) for providing the LTR:GUS transgenic lines. We thank D. Gilmer (Institut de Biologie Moléculaire des Plantes) for providing antiserum to GFP. This project was supported by a core grant from ETH-Z and a grant from the Swiss National Foundation Genetics of miRNA Action and Biogenesis (31003A_132907). A.M.-O. is supported by a PhD fellowship from the ETH-Z foundation.

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Author notes

  1. Antoine Martin

    Present address: Present address: Institut de Biologie Intégrative des Plantes (IBIP), Biochimie et Physiologie Moléculaire des Plantes, UMR 5004 CNRS, Institut National de la Recherche Agronomique (INRA), SupAgro, UM2, Montpellier, France.,

  2. Antonin Marchais and Mathilde Etcheverry: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, Swiss Federal Institute of Technology (ETH-Z), Zurich, Switzerland

    Arturo Marí-Ordóñez, Antonin Marchais & Olivier Voinnet

  2. Life Science Zurich Graduate School, Molecular Life Science Program, University of Zurich, Zurich, Switzerland

    Arturo Marí-Ordóñez & Olivier Voinnet

  3. Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Centre National de la Recherche Scientifique (CNRS) Unité Mixte de Recherche (UMR) 8197 and Institut National de la Santé et de la Recherche Médicale (INSERM) U1024, Paris, France

    Mathilde Etcheverry, Antoine Martin & Vincent Colot

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  1. Arturo Marí-Ordóñez
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Contributions

O.V. and A.M.-O. conceived and designed the experiments, helped by V.C. on experiments involving ddm1-mutant epiRILs. A.M.-O., M.E. and A. Martin performed the experiments. O.V., V.C., A.M.-O. and M.E. analyzed the data. A. Marchais performed computer and statistical analyses. O.V. and A.M.-O. wrote the manuscript.

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Correspondence to Olivier Voinnet.

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Marí-Ordóñez, A., Marchais, A., Etcheverry, M. et al. Reconstructing de novo silencing of an active plant retrotransposon. Nat Genet 45, 1029–1039 (2013). https://doi.org/10.1038/ng.2703

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