Immunity onset alters plant chromatin and utilizes EDA16 to regulate oxidative homeostasis

PLoS Pathog. 2021 May 20;17(5):e1009572. doi: 10.1371/journal.ppat.1009572. eCollection 2021 May.

Abstract

Perception of microbes by plants leads to dynamic reprogramming of the transcriptome, which is essential for plant health. The appropriate amplitude of this transcriptional response can be regulated at multiple levels, including chromatin. However, the mechanisms underlying the interplay between chromatin remodeling and transcription dynamics upon activation of plant immunity remain poorly understood. Here, we present evidence that activation of plant immunity by bacteria leads to nucleosome repositioning, which correlates with altered transcription. Nucleosome remodeling follows distinct patterns of nucleosome repositioning at different loci. Using a reverse genetic screen, we identify multiple chromatin remodeling ATPases with previously undescribed roles in immunity, including EMBRYO SAC DEVELOPMENT ARREST 16, EDA16. Functional characterization of the immune-inducible chromatin remodeling ATPase EDA16 revealed a mechanism to negatively regulate immunity activation and limit changes in redox homeostasis. Our transcriptomic data combined with MNase-seq data for EDA16 functional knock-out and over-expressor mutants show that EDA16 selectively regulates a defined subset of genes involved in redox signaling through nucleosome repositioning. Thus, collectively, chromatin remodeling ATPases fine-tune immune responses and provide a previously uncharacterized mechanism of immune regulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism*
  • Arabidopsis / genetics
  • Arabidopsis / immunology
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Chromatin / genetics
  • Chromatin Assembly and Disassembly / immunology*
  • DNA Helicases / genetics
  • DNA Helicases / metabolism*
  • Homeostasis
  • Nicotiana / genetics
  • Nicotiana / immunology
  • Nicotiana / physiology
  • Nucleosomes / genetics
  • Oxidation-Reduction
  • Oxidative Stress
  • Plant Diseases / immunology*
  • Plant Diseases / microbiology
  • Plant Immunity / genetics*
  • Pseudomonas syringae / immunology*

Substances

  • Arabidopsis Proteins
  • Chromatin
  • Nucleosomes
  • Adenosine Triphosphatases
  • AT1G61140 protein, Arabidopsis
  • DNA Helicases