H3K4me2 orchestrates H2A.Z and Polycomb repressive marks in Arabidopsis

The dimethylation of histone H3 lysine 4 (H3K4me2) plays an important role in developmental phase transitions in plants, such as regeneration from the callus and the initiation of flowering. H3K4me2 in plants is correlated with transcriptionally repressed states, which can be accounted for by transcription-coupled active H3K4me2 demethylation, but the converse molecular pathway by which H3K4me2 represses transcription remains largely unexplored. Here, we show that H3K4me2 colocalizes with the H2A variant H2A.Z and H2A ubiquitination (H2Aub). Our genetic analyses reveal that H3K4me2 functions upstream but not downstream of these marks. H3K4me2 also partially colocalizes with the facultative heterochromatin mark H3K27me3, and loss of H3K4me2 causes a decrease in the colocalized H3K27me3. Interestingly, in genes with diel H3K4me2 oscillation, H3K4me2 oscillates in antiphase with transcription but in phase with H2A.Z. In addition, the genetic manipulation of H3K4me2 affects the oscillating profiles of H2A.Z, suggesting the efficient relay from H3K4me2 to H2A.Z. Notably, the diel oscillation of H2Aub is much weaker than that of H2A.Z despite the overall similarity in their distributions. These results suggest that H3K4me2 orchestrates H2A.Z and H2Aub with distinct dynamics. We propose that H3K4me2 promotes stepwise progression of chromatin toward repressive states in plants.