Histone occupancy-dependent and -independent removal of H3K27 trimethylation at cold-responsive genes in Arabidopsis

Trimethylation of histone H3 at lysine 27 (H3K27me3) is a histone marker that is present in inactive gene loci in both plants and animals. Transcription of some of the genes with H3K27me3 should be induced by internal or external cues, yet the dynamic fate of H3K27me3 in these genes during transcriptional regulation is poorly understood in plants. Here we show that H3K27me3 in two cold-responsive genes, COR15A and ATGOLS3, decreases gradually in Arabidopsis during exposure to cold temperatures. We found that removal of H3K27me3 can occur by both histone occupancy-dependent and -independent mechanisms. Upon cold exposure, histone H3 levels decreased in the promoter regions of COR15A and ATGOLS3 but not in their transcribed regions. When we returned cold-exposed plants to normal growth conditions, transcription of COR15A and ATGOLS3 was completely repressed to the initial level before cold exposure in 1 day. In contrast, plants still maintained the cold-triggered decrease in H3K27me3 at COR15A and ATGOLS3, but this decrease did not enhance transcriptional induction of the two genes upon re-exposure to cold. Taken together, these results indicate that gene activation is not inhibited by H3K27me3 itself but rather leads to removal of H3K27me3, and that H3K27me3 can be inherited at a quantitative level, thereby serving as a memory marker for recent transcriptional activity in Arabidopsis.