The Arabidopsis active demethylase ROS1 cis-regulates defense genes by erasing DNA methylation at promoter-regulatory regions
- IBENS-CNRS, France
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.
Article and author information
Author details
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
- Daniel Zilberman, John Innes Centre, United Kingdom
Version history
- Received: September 10, 2020
- Accepted: January 19, 2021
- Accepted Manuscript published: January 20, 2021 (version 1)
- 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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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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