Dynamics of H3K4me3 Chromatin Marks Prevails over H3K27me3 for Gene Regulation during Flower Morphogenesis in Arabidopsis thaliana

Plant life-long organogenesis involves sequential, time and tissue specific expression of developmental genes. This requires activities of Polycomb Group (PcG) and trithorax Group complexes (trxG), respectively responsible for repressive Histone 3 trimethylation at lysine 27 (H3K27me3) and activation-related Histone 3 trimethylation at lysine 4 (H3K4me3). However, the genome-wide dynamics in histone modifications that occur during developmental processes have remained elusive. Here, we report the distributions of H3K27me3 and H3K4me3 along with expression changes, in a developmental series including Arabidopsis thaliana leaf and three stages of flower development. We found that chromatin mark levels are highly dynamic over the time series on nearly half of all Arabidopsis genes. Moreover, during early flower morphogenesis, changes in H3K4me3 prevail over changes in H3K27me3 and quantitatively correlate with expression changes, while H3K27me3 changes occur later. Notably, we found that H3K4me3 increase during the early activation of PcG target genes while H3K27me3 level remain relatively constant at the locus. Our results reveal that H3K4me3 predicts changes in gene expression better than H3K27me3, unveil unexpected chromatin mechanisms at gene activation and underline the relevance of tissue-specific temporal epigenomics.