Trimethylation of histone H3 lysine 27 (H3K27me3) is critically important for the normal development of animals. The Polycomb-group (PcG) protein complexes PhoRC, PRC1, and PRC2 collectively establish and maintain H3K27me3 at ~400 and ~2,000 genes in Drosophila
and mammals, respectively [1
]. In Drosophila
, PRC1 and PRC2 are recruited to nucleosome-depleted regions of the genome called Polycomb response elements (PREs) primarily through the sequence-specific binding activity of Pho [1
]. The PRC2 complex then catalyzes the trimethylation of H3K27, whereas the PRC1 complex is required for the bidirectional spreading of H3K27me3 from PREs to the adjacent regions, presumably until an insulator is encountered. As a result, H3K27me3 forms broad domains in Drosophila
and mammals that can span up to hundreds of kilobases and cover multiple genes, maintaining them in a transcriptionally suppressed state at appropriate developmental stages [1
]. The observation that H3K27me3 target genes are enriched for transcription factors underscores the importance of this histone modification in regulating animal development [1
Plants also contain ample amounts of H3K27me3, accounting for ~5% of the canonical histone H3.1, but trimethylation is undetectable on the histone variant H3.2 (referred to as H3.3 in Drosophila
) that is predicted to be associated with actively transcribed genes [13
]. Furthermore, Arabidopsis
mutants defective in H3K27me3 exhibit severe developmental abnormalities [15
], and the repression of several important developmental patterning genes in Arabidopsis
, such as FLOWERING LOCUS C (FLC), AGAMOUS,
requires H3K27me3 [19
]. It is therefore likely that the silencing function of H3K27me3 is conserved between plants and animals and that H3K27me3 also plays essential roles in regulating normal plant development.
However, several important questions regarding the patterning and function of H3K27me3 in plants remain unanswered. For example, the extent to which H3K27me3 regulates plant gene expression on a genome-wide scale is unknown. Thus far, only seven plant genes have been shown to be associated with H3K27me3, including FLC, AGAMOUS, MEDEA, SHOOT MERISTEMLESS (STM), PHERES1, FUSCA3,
and AGAMOUS-LIKE 19 (AGL19)
]. In addition, whereas plants have homologs of each of the PRC2 components, they do not encode components of PRC1 or PhoRC, and it is therefore not clear whether H3K27me3 is established and maintained by similar mechanisms in plants and animals [28
]. Furthermore, the relationship between H3K27me3 and other important epigenetic pathways in plants such as DNA methylation and RNA interference (RNAi) has not been determined.
To begin to address these questions, we identified regions containing H3K27me3 in the Arabidopsis genome using high-resolution whole-genome tiling microarrays. We found that H3K27me3 regulates an unexpectedly large number of genes (~4,400) in Arabidopsis, including numerous transcription factors. In addition, we present evidence that H3K27me3 functions independently of DNA methylation or RNAi. Furthermore, several important differences were observed between the patterning of H3K27me3 in Arabidopsis and Drosophila, suggesting that distinct mechanisms may underlie the establishment and maintenance of H3K27me3 in plants and animals.