H3K27me3 Profiling of the Endosperm Implies Exclusion of Polycomb Group Protein Targeting by DNA Methylation

Abstract

Polycomb group (PcG) proteins act as evolutionary conserved epigenetic mediators of cell identity because they repress transcriptional programs that are not required at particular developmental stages. Each tissue is likely to have a specific epigenetic profile, which acts as a blueprint for its developmental fate. A hallmark for Polycomb Repressive Complex 2 (PRC2) activity is trimethylated lysine 27 on histone H3 (H3K27me3). In plants, there are distinct PRC2 complexes for vegetative and reproductive development, and it was unknown so far whether these complexes have target gene specificity. The FERTILIZATION INDEPENDENT SEED (FIS) PRC2 complex is specifically expressed in the endosperm and is required for its development; loss of FIS function causes endosperm hyperproliferation and seed abortion. The endosperm nourishes the embryo, similar to the physiological function of the placenta in mammals. We established the endosperm H3K27me3 profile and identified specific target genes of the FIS complex with functional roles in endosperm cellularization and chromatin architecture, implicating that distinct PRC2 complexes have a subset of specific target genes. Importantly, our study revealed that selected transposable elements and protein coding genes are specifically targeted by the FIS PcG complex in the endosperm, whereas these elements and genes are densely marked by DNA methylation in vegetative tissues, suggesting that DNA methylation prevents targeting by PcG proteins in vegetative tissues.

Genome-wide redistribution of H3K27me3 is linked to genotoxic stress and defective growth

“…This may also be the case in E. festucae, where deletion of the H3K27 MTase ΔezhB does not rescue the growth defects of the H3K9 MTase-deficient mutant ΔclrD (22). In plants and animals, cross-talk between different heterochromatin components and the Pc system has been linked to cell type-specific changes in chromatin architecture, raising the possibility that different heterochromatin-based mechanisms could regulate H3K27me3 in different cells even within the same organism (71,81,82).…”

Identification and Characterization of an Epi-Allele of FIE1 Reveals a Regulatory Linkage between Two Epigenetic Marks in Rice

“…The loss-of-function mutants of IBM1 showed ectopic CHG methylation and H3K9me2 in thousands of genes (Miura et al, 2009a;Inagaki et al, 2010). Recent studies discovered that endosperm H3K27me3 profile identified some transposable elements and protein coding genes that contained a lower level of DNA methylation and were subjected to H3K27me3, whereas these sequences contain dense DNA methylation and are absent of H3K27me3 in vegetative tissues, suggesting that DNA methylation prevents the establishment of H3K27me3 at targets in vegetative tissues (Weinhofer et al, 2010).…”

Imprinting meets genomics: new insights and new challenges

“…This and another study concluded that PRC2 can regulate maternal and paternal alleles of MEGs and maternal alleles of PEGs [5] [6]. In endosperm, paternal alleles of PEGs might be protected from PRC2 repression because of DNA methylation continuously present at those loci [25].…”

“…Reduced DNA methylation levels in the endosperm might enable targeting of Polycomb group proteins to selected loci, catalyzing trimethylation of lysine 27 on histone H3 (H3K27me3), a hallmark of silent chromatin [25]. Figure 2C).…”