Genome-wide profiling of histone H3 lysine 9 acetylation and dimethylation in Arabidopsis reveals correlation between multiple histone marks and gene expression

Lysine residue 9 of histone H3 can either be acetylated or mono-, di-, or tri-methylated. These epigenetic states have a diverse impact on regulating gene transcriptional activity and chromatin organization. H3K9ac is invariably correlated with transcriptional activation, whereas H3K9me2 has been reported to be mainly located in constitutive heterochromatin in Arabidopsis. Here, we present epigenetic landscapes for histone H3 lysine 9 acetylation (H3K9ac) and dimethylation (H3K9me2) in Arabidopsis seedlings. The results show that H3K9ac targeted 5,206 non-transposable element (non-TE) genes and 321 transposable elements (TEs), whereas H3K9me2 targeted 2,281 TEs and 1,112 non-TE genes. H3K9ac was biased towards the 5′ end of genes and peaked at the ATG position, while H3K9me2 tended to span the entire gene body. H3K9ac correlated with high gene expression, while H3K9me2 correlated with low expression. Analyses of H3K9ac and H3K9me2 with the available datasets of H3K27me3 and DNA methylation revealed a correlation between the occurrence of multiple epigenetic modifications and gene expression. Genes with H3K9ac alone were actively transcribed, while genes that were also modified by either H3K27me3 or DNA methylation showed a lower expression level, suggesting that a combination of repressive marks weakened the positive regulatory effect of H3K9ac. Furthermore, we observed a significant increase of the H3K9ac modification level of selected target genes in hda19 (histone deacetylase 19) mutant seedlings, which indicated that HDA19 plays an important role in regulating the level of H3K9ac and thereby influencing the transcriptional activity in young seedlings.