JASMONATE-ZIM DOMAIN proteins engage Polycomb chromatin modifiers to modulate Jasmonate signaling in Arabidopsis

Jasmonate (JA) regulates various aspects of plant growth and development and stress responses, with prominent roles in male reproductive development and defenses against herbivores and necrotrophic pathogens. JASMONATE-ZIM DOMAIN (JAZ) proteins are key regulators in the JA signaling pathway and function to repress the expression of JA-responsive genes. Here, we show that JAZ proteins directly interact with several chromatin-associated Polycomb proteins to mediate repressive chromatin modifications at JA-responsive genes and, thus, their transcriptional repression in Arabidopsis. Genetic analyses revealed that the developmental defects, including anther and pollen abnormalities, resulting from loss or block of JA signaling were partially rescued by loss of Polycomb protein-mediated chromatin silencing (Polycomb repression). We further found that JAZ-mediated transcriptional repression during anther and pollen development requires Polycomb proteins at four key regulatory loci. Analysis of genome-wide occupancy of a Polycomb factor and transcriptome reprogramming in response to JA revealed that Polycomb repression is involved in the repression of various JA-responsive genes. Taken together, our study reveals an important chromatin-based mechanism for JAZ-mediated transcriptional repression and JA signaling in plants.