H3K27me3 and H2A.Z prime cold regulated genes, and their remodelling governs plant cold response

To elucidate the contribution of chromatin modifications in plant cold response, we performed ChIP-seq for H3K27me3 and H2A.Z in Arabidopsis exposed to short-term cold. We combined our epigenetic data with NET-seq to investigate the direct transcriptional effects of histone marks. Prior to any stress cue, cold regulated genes share a similar chromatin environment with high H2A.Z and H3K27me3. H3K27me3 levels do not correlate with transcriptional activity or elongation speed. However, REF6-mediated reduction of H3K27me3 is essential for regulation of cold controlled genes. H2A.Z occupancy changes revealed a negative correlation between cold-induced changes to H2A.Z and RNAPII activity at differentially expressed genes. Importantly, changing H2A.Z levels preceded transcriptional changes, indicating that the variant functions as a critical cold-induced switch. Further, our data suggests that high H2A.Z levels slow down RNAPII. Thus, H2A.Z is essential for the transcriptional response and a decreased H3K27me3 level is important for the genomic adaptation to cold.