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

• Published in: PLoS pathogens 2021-05, Vol.17 (5), p.e1009572-e1009572
• Main Authors: Pardal, Alonso J, Piquerez, Sophie J M, Dominguez-Ferreras, Ana, Frungillo, Lucas, Mastorakis, Emmanouil, Reilly, Emma, Latrasse, David, Concia, Lorenzo, Gimenez-Ibanez, Selena, Spoel, Steven H, Benhamed, Moussa, Ntoukakis, Vardis
• Format: Article
• Language: English
• Subjects: Adenosine triphosphatase; Adenosine Triphosphatases - genetics; Adenosine Triphosphatases - metabolism; Arabidopsis - genetics; Arabidopsis - immunology; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Biology and Life Sciences; Calcium influx; Chromatin; Chromatin - genetics; Chromatin Assembly and Disassembly - immunology; Chromatin remodeling; Crop diseases; Datasets; Deoxyribonucleic acid; DNA; DNA Helicases - genetics; DNA Helicases - metabolism; DNA methylation; DNA sequencing; Gene expression; Gene sequencing; Genetic aspects; Genetic screening; Genomes; Hardiness; Homeostasis; Host-bacteria relationships; Immune response; Immunity; Kinases; Medicine and Health Sciences; Nicotiana - genetics; Nicotiana - immunology; Nicotiana - physiology; Nuclease; Nucleosomes; Nucleosomes - genetics; Oxidation-Reduction; Oxidative Stress; Pathogens; Plant Diseases - immunology; Plant Diseases - microbiology; Plant immunity; Plant Immunity - genetics; Plant viruses; Plants; Properties; Proteins; Pseudomonas syringae - immunology; Reactive oxygen species; Research and Analysis Methods; Salicylic acid; Transcription; Virus diseases of plants
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1009572

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.