A J-protein-licensed CHD3 chromatin remodeling complex promotes H3K27me3 spreading to maintain cell identity in plants

Abstract

Stable inheritance of epigenetic states is essential for cellular identity and developmental robustness and requires ATP-dependent chromatin remodeling, yet the molecular composition and regulatory mechanisms of plant CHD3 chromatin remodelers have remained unknown. Here we show that the Arabidopsis CHD3 remodeler PICKLE (PKL) assembles with a defined set of J-domain proteins (JDPs) to form stable CHD3 chromatin remodeling complexes in plants that are compositionally distinct from their animal counterparts. Loss of JDPs phenocopies pkl mutants, and JDPs are required for nucleosome densification and H3K27me3 spreading at thousands of Polycomb target genes. Mechanistically, JDPs perform dual functions by promoting PKL protein stability while directly stimulating PKL chromatin remodeling activity through their plant-specific DUF3444 domain that binds the N-terminal tail of histone H3. Deletion of the DUF3444 domain severely impairs PKL remodeling activity without disrupting complex assembly, leading to defective H3K27me3 spreading, impaired facultative heterochromatin maintenance, and loss of cell identity. Together, our findings define plant CHD3 chromatin remodeling complexes and reveal a mechanism that regulates CHD3-mediated chromatin remodeling to support the propagation of repressive chromatin states in plants.