A new role for histone demethylases in the maintenance of plant genome integrity

  1. Javier Antunez-Sanchez
  2. Matthew Naish
  3. Juan Sebastian Ramirez-Prado
  4. Sho Ohno
  5. Ying Huang
  6. Alexander Dawson
  7. Korawit Opassathian
  8. Deborah Manza-Mianza
  9. Federico Ariel
  10. Cecile Raynaud
  11. Anjar Wibowo
  12. Josquin Daron
  13. Minako Ueda
  14. David Latrasse
  15. R Keith Slotkin
  16. Detlef Weigel
  17. Moussa Benhamed  Is a corresponding author
  18. Jose Gutierrez-Marcos  Is a corresponding author
  1. University of Warwick, United Kingdom
  2. Institute of Plant Sciences Paris Saclay, France
  3. Max Planck Institute for Developmental Biology, Germany
  4. The Ohio State University, United States
  5. Nagoya University, Japan
  6. Donald Danforth Plant Science Center, United States
  7. Université Paris Saclay, France

Abstract

Histone modifications deposited by the Polycomb repressive complex 2 (PRC2) play a critical role in the control of growth, development, and adaptation to environmental fluctuations of most multicellular eukaryotes. The catalytic activity of PRC2 is counteracted by Jumonji-type (JMJ) histone demethylases, which shapes the genomic distribution of H3K27me3. Here, we show that two JMJ histone demethylases in Arabidopsis, EARLY FLOWERING 6 (ELF6) and RELATIVE OF EARLY FLOWERING 6 (REF6), play distinct roles in H3K27me3 and H3K27me1 homeostasis. We show that failure to reset these chromatin marks during sexual reproduction results in the transgenerational inheritance of histone marks, which cause a loss of DNA methylation at heterochromatic loci and transposon activation. Thus, Jumonji-type histone demethylases play a dual role in plants by helping to maintain transcriptional states through development and safeguard genome integrity during sexual reproduction.

Data availability

Sequence data (BS-seq, RNA-seq and ChiP-seq) that support the findings of this study have been deposited at the European Nucleotide Archive (ENA) under the accession code PRJEB36508.

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

Article and author information

Author details

  1. Javier Antunez-Sanchez

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  2. Matthew Naish

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8977-1295
  3. Juan Sebastian Ramirez-Prado

    Plant Sciences, Institute of Plant Sciences Paris Saclay, Orsay Cedex, France
    Competing interests
    No competing interests declared.
  4. Sho Ohno

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  5. Ying Huang

    Plant Sciences, Institute of Plant Sciences Paris Saclay, Orsay Cedex, France
    Competing interests
    No competing interests declared.
  6. Alexander Dawson

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  7. Korawit Opassathian

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  8. Deborah Manza-Mianza

    Plant Sciences, Institute of Plant Sciences Paris Saclay, Gif-sur-yvette, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3374-0200
  9. Federico Ariel

    Plant Sciences, Institute of Plant Sciences Paris Saclay, Orsay Cedex, France
    Competing interests
    No competing interests declared.
  10. Cecile Raynaud

    Plant Sciences, Institute of Plant Sciences Paris Saclay, Orsay Cedex, France
    Competing interests
    No competing interests declared.
  11. Anjar Wibowo

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    No competing interests declared.
  12. Josquin Daron

    Department of Molecular Genetics, The Ohio State University, Columbus, United States
    Competing interests
    No competing interests declared.
  13. Minako Ueda

    Institute of Transformative Bio-Molecules, Nagoya University, Nagoya, Japan
    Competing interests
    No competing interests declared.
  14. David Latrasse

    Plant Sciences, Institute of Plant Sciences Paris Saclay, Orsay Cedex, France
    Competing interests
    No competing interests declared.
  15. R Keith Slotkin

    Donald Danforth Plant Science Center, St Louis, United States
    Competing interests
    No competing interests declared.
  16. Detlef Weigel

    Department of Molecular Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    Detlef Weigel, Deputy/Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2114-7963
  17. Moussa Benhamed

    Plant Biology, Université Paris Saclay, Orsayffff, France
    For correspondence
    moussa.benhamed@u-psud.fr
    Competing interests
    No competing interests declared.
  18. Jose Gutierrez-Marcos

    School of Life Sciences, University of Warwick, Coventry, United Kingdom
    For correspondence
    j.f.gutierrez-marcos@warwick.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5441-9080

Funding

European Commission (AUREATE)

  • Jose Gutierrez-Marcos

Biotechnology and Biological Sciences Research Council (BB/L003023/1,BB/N005279/1,BB/N00194X/1 and BB/P02601X/1)

  • Jose Gutierrez-Marcos

Japan Society for the Promotion of Science (JP19H05676)

  • Minako Ueda

Agence Nationale de la Recherche (EpiGen)

  • Moussa Benhamed

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

Reviewing Editor

  1. Pil Joon Seo, Seoul National University, Korea (South), Republic of

Publication history

  1. Received: May 4, 2020
  2. Accepted: October 26, 2020
  3. Accepted Manuscript published: October 27, 2020 (version 1)
  4. Version of Record published: November 17, 2020 (version 2)

Copyright

© 2020, Antunez-Sanchez 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. Javier Antunez-Sanchez
  2. Matthew Naish
  3. Juan Sebastian Ramirez-Prado
  4. Sho Ohno
  5. Ying Huang
  6. Alexander Dawson
  7. Korawit Opassathian
  8. Deborah Manza-Mianza
  9. Federico Ariel
  10. Cecile Raynaud
  11. Anjar Wibowo
  12. Josquin Daron
  13. Minako Ueda
  14. David Latrasse
  15. R Keith Slotkin
  16. Detlef Weigel
  17. Moussa Benhamed
  18. Jose Gutierrez-Marcos
(2020)
A new role for histone demethylases in the maintenance of plant genome integrity
eLife 9:e58533.
https://doi.org/10.7554/eLife.58533

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