The Arabidopsis active demethylase ROS1 cis-regulates defense genes by erasing DNA methylation at promoter-regulatory regions

Abstract

Active DNA demethylation has emerged as an important regulatory process of plant and mammalian immunity. However, very little is known about the mechanisms by which active demethylation controls transcriptional immune reprogramming and disease resistance. Here, we first show that the Arabidopsis active demethylase ROS1 promotes basal resistance towards Pseudomonas syringae by antagonizing RNA-directed DNA methylation (RdDM). Furthermore, we find that ROS1 facilitates the flagellin-triggered induction of the disease resistance gene RMG1 by limiting RdDM at the 3' boundary of a remnant RC/Helitron transposable element (TE) embedded in its promoter. We further identify flagellin-responsive ROS1 putative primary targets, and show that at a subset of promoters, ROS1 erases methylation at discrete regions exhibiting WRKY transcription factors (TFs) binding. In particular, we demonstrate that ROS1 removes methylation at the orphan immune receptor RLP43 promoter, to ensure DNA binding of WRKY TFs. Finally, we show that ROS1-directed demethylation of the RMG1 and RLP43 promoters is causal for both flagellin responsiveness of these genes and for basal resistance. Overall, these findings significantly advance our understanding of how active demethylases shape transcriptional immune reprogramming to enable antibacterial resistance.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all main figures and for supplemental figures. Sequencing data have been deposited in SRA under the accession code SRP133028.

The following data sets were generated

Article and author information

Author details

  1. Thierry Halter

    Biology, IBENS-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Jingyu Wang

    Biology, IBENS-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Delase Amesefe

    Biology, IBENS-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Emmanuelle Lastrucci

    Biology, IBENS-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Magali Charvin

    Biology, IBENS-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Meenu Singla Rastogi

    Biology, IBENS-CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Lionel Navarro

    Biology, IBENS-CNRS, Paris, France
    For correspondence
    lionel.navarro@ens.psl.eu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1083-9478

Funding

H2020 European Research Council (Silencing & Immunity (281749))

  • Lionel Navarro

Agence Nationale de la Recherche (NEPRHON (ANR-18-CE20-0020))

  • Lionel Navarro

H2020 Marie Skłodowska-Curie Actions (EU Project 661715 - BASILA)

  • Thierry Halter

Fondation Pierre-Gilles de Gennes pour la recherche

  • Thierry Halter

Agence Nationale de la Recherche (ANR-10-IDEX-0001-02PSL)

  • Lionel Navarro

Agence Nationale de la Recherche (ANR-10-LABX-54 MEMOLIFE)

  • Lionel Navarro

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

Reviewing Editor

  1. Daniel Zilberman, John Innes Centre, United Kingdom

Publication history

  1. Received: September 10, 2020
  2. Accepted: January 19, 2021
  3. Accepted Manuscript published: January 20, 2021 (version 1)
  4. Version of Record published: February 12, 2021 (version 2)

Copyright

© 2021, Halter 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. Thierry Halter
  2. Jingyu Wang
  3. Delase Amesefe
  4. Emmanuelle Lastrucci
  5. Magali Charvin
  6. Meenu Singla Rastogi
  7. Lionel Navarro
(2021)
The Arabidopsis active demethylase ROS1 cis-regulates defense genes by erasing DNA methylation at promoter-regulatory regions
eLife 10:e62994.
https://doi.org/10.7554/eLife.62994

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