H3K4me1 directs H3K36me2 and H3K36me3 deposition in land plants.

Monomethylation of histone 3 lysine 4 (H3K4me1) marks enhancers in mammals. However, the function of H3K4me1 in plants remains largely unclear. Here, we present the genome-wide distribution of H3K4me1 in diverse species across evolution, revealing a distinctive H3K4me1 distribution pattern in land plants. To explore the function of H3K4me1 in plants, we identified an H3K4me1-specific reader protein, Early heading date 3 (Ehd3), and solved the structure of Ehd3 in complex with the H3K4me1 peptide, revealing a unique binding module differing from the previously reported PHD finger proteins. We further identified an Ehd3-binding protein, SET domain group 724 (SDG724), and the deletion of either Ehd3 or SDG724 caused similar defects in plant phenotype and changes in transcriptome and epigenome profiles. Both Ehd3 and SDG724 are enriched at chromatin regions marked by H3K4me1 but not H3K4me2 or H3K4me3. Ehd3 activates the H3K36 methyltransferase SDG724, and H3K36me2/me3 are colocalized with H3K4me1 in the genomes of the examined land plants. Collectively, our results reveal that H3K4me1 directs the establishment of H3K36me2 and H3K36me3 in land plants.