Distinct chromatin signatures in the Arabidopsis male gametophyte

Epigenetic reprogramming in the germline contributes to the erasure of epigenetic inheritance across generations in mammals but remains poorly characterized in plants. Here we profiled histone modifications throughout Arabidopsis male germline development. We find that the sperm cell has widespread apparent chromatin bivalency, which is established by the acquisition of H3K27me3 or H3K4me3 at pre-existing H3K4me3 or H3K27me3 regions, respectively. These bivalent domains are associated with a distinct transcriptional status. Somatic H3K27me3 is generally reduced in sperm, while dramatic loss of H3K27me3 is observed at only similar to 700 developmental genes. The incorporation of the histone variant H3.10 facilitates the establishment of sperm chromatin identity without a strong impact on resetting of somatic H3K27me3. Vegetative nuclei harbor thousands of specific H3K27me3 domains at repressed genes, while pollination-related genes are highly expressed and marked by gene body H3K4me3. Our work highlights putative chromatin bivalency and restricted resetting of H3K27me3 at developmental regulators as key features in plant pluripotent sperm.

Automated summary

Epigenetic reprogramming in plant germline cells involves widespread chromatin bivalency and restricted resetting of H3K27me3 at developmental regulators. The incorporation of histone variant H3.10 helps establish the unique chromatin identity of sperm without impacting somatic H3K27me3 resetting. Additionally, specific H3K27me3 domains are present at repressed genes in vegetative nuclei, while pollination-related genes are highly expressed and marked by gene body H3K4me3.