Repression of CHROMOMETHYLASE 3 prevents epigenetic collateral damage in Arabidopsis

  1. Ranjith K Papareddy
  2. Katalin Páldi
  3. Anna D Smolka
  4. Patrick Hüther
  5. Claude Becker
  6. Michael D Nodine  Is a corresponding author
  1. Gregor Mendel Institute, Austria
  2. Gregor Mendel Institute; LMU Biocenter, Austria
  3. Gregor Mendel Institute; LMU Biocenter, Germany
  4. Gregor Mendel Institute; Wageningen University, Austria

Abstract

DNA methylation has evolved to silence mutagenic transposable elements (TEs) while typically avoiding the targeting of endogenous genes. Mechanisms that prevent DNA methyltransferases from ectopically methylating genes are expected to be of prime importance during periods of dynamic cell cycle activities including plant embryogenesis. However, virtually nothing is known regarding how DNA methyltransferase activities are precisely regulated during embryogenesis to prevent the induction of potentially deleterious and mitotically stable genic epimutations. Here, we report that microRNA-mediated repression of CHROMOMETHYLASE 3 (CMT3) and the chromatin features that CMT3 prefers help prevent ectopic methylation of thousands of genes during embryogenesis that can persist for weeks afterwards. Our results are also consistent with CMT3-induced ectopic methylation of promoters or bodies of genes undergoing transcriptional activation reducing their expression. Therefore, the repression of CMT3 prevents epigenetic collateral damage on endogenous genes. We also provide a model that may help reconcile conflicting viewpoints regarding the functions of gene-body methylation that occurs in nearly all flowering plants.

Data availability

All sequencing data generated in this study are publicly available at the National Center for Biotechnology Information Gene Expression Omnibus (NCBI GEO, https://www.ncbi.nlm.nih.gov/geo/) under accession number GSE171198.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Ranjith K Papareddy

    Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  2. Katalin Páldi

    Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Anna D Smolka

    Gregor Mendel Institute, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  4. Patrick Hüther

    Austrian Academy of Sciences, Vienna Biocenter, Gregor Mendel Institute; LMU Biocenter, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  5. Claude Becker

    Genetics, Gregor Mendel Institute; LMU Biocenter, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3406-4670
  6. Michael D Nodine

    Gregor Mendel Institute; Wageningen University, Vienna, Austria
    For correspondence
    michael.nodine@wur.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6204-8857

Funding

H2020 European Research Council (637888)

  • Michael D Nodine

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Richard Amasino, University of Wisconsin Madison, United States

Publication history

  1. Received: April 13, 2021
  2. Accepted: July 21, 2021
  3. Accepted Manuscript published: July 23, 2021 (version 1)
  4. Accepted Manuscript updated: July 26, 2021 (version 2)
  5. Version of Record published: August 9, 2021 (version 3)

Copyright

© 2021, Papareddy et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Ranjith K Papareddy
  2. Katalin Páldi
  3. Anna D Smolka
  4. Patrick Hüther
  5. Claude Becker
  6. Michael D Nodine
(2021)
Repression of CHROMOMETHYLASE 3 prevents epigenetic collateral damage in Arabidopsis
eLife 10:e69396.
https://doi.org/10.7554/eLife.69396

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