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Global analysis of H3K4me3/H3K27me3 in Brachypodium distachyon reveals VRN3 as critical epigenetic regulation point in vernalization and provides insights into epigenetic memory.

Vernalization, the requirement of plants for long-term exposure to low environmental temperature for flowering, is an epigenetic phenomenon. Histone modification regulation has been revealed in vernalization, but is limited to key genes. Now, we know that VRN1 is epigenetically critical for monocots. Genome-wide analysis is still unavailable, however. We performed chromatin immunoprecipitation-sequencing for H3K4me3/H3K27me3 in Brachypodium distachyon to obtain a global view of histone modifications in vernalization on a genome-wide scale and for different pathways/genes. Our data showed that H3K4me3 and H3K27me3 play distinct roles in vernalization. Unlike H3K4me3, H3K27me3 exhibited regional regulation, showed main regulation targets in vernalization and contributed to epigenetic memory. For genes in four flowering regulation pathways, only FT2 (functional ortholog of VRN3 in B. distachyon) and VRN1 showed coordinated changes in H3K4me3/H3K27me3. The epigenetic response at VRN3 was weaker under short-day than under long-day conditions. VRN3 was revealed as an epigenetic regulation point integrating vernalization and day length signals. We globally identified genes maintaining vernalization-induced epigenetic changes. Most of these genes showed dose-dependent vernalization responses, revealing a quantitative 'recording system' for vernalization. Our studies shed light on the epigenetic role of VRN3 and H3K4me3/H3K27me3 in vernalization and reveal genes underlying epigenetic memory, laying the foundation for further study.