Parental epigenetic asymmetry of PRC 2‐mediated histone modifications in the Arabidopsis endosperm

Abstract

Parental genomes in the endosperm are marked by differential DNA methylation and are therefore epigenetically distinct. This epigenetic asymmetry is established in the gametes and maintained after fertilization by unknown mechanisms. In this manuscript, we have addressed the key question whether parentally inherited differential DNA methylation affects de novo targeting of chromatin modifiers in the early endosperm. Our data reveal that polycomb-mediated H3 lysine 27 trimethylation (H3K27me3) is preferentially localized to regions that are targeted by the DNA glycosylase DEMETER (DME), mechanistically linking DNA hypomethylation to imprinted gene expression. Our data furthermore suggest an absence of de novo DNA methylation in the early endosperm, providing an explanation how DME-mediated hypomethylation of the maternal genome is maintained after fertilization. Lastly, we show that paternal-specific H3K27me3-marked regions are located at pericentromeric regions, suggesting that H3K27me3 and DNA methylation are not necessarily exclusive marks at pericentromeric regions in the endosperm.

Endosperm and Imprinting, Inextricably Linked

“…Their findings suggest that DNA methylation is dynamic during endosperm development. CHH methylation is absent from endosperm at 4 d after pollination (Moreno-Romero et al, 2016). This agrees with gene expression profiling of laser capture dissected endosperm tissue that indicates low expression of the RdDM components in the endosperm until the heart stage (Belmonte et al, 2013) and with observations on the expression of methyltransferase reporter genes (Jullien et al, 2012).…”

“…By 6 d after pollination CHH methylation is well established in the endosperm (Pignatta et al, 2014), indicating an increase in de novo DNA methylation activity. Moreno-Romero et al (2016) also demonstrated that maternal allele-specific histone H3 trimethylation at Lys-27 (H3K27me3) is located at sites demethylated by DME. H3K27me3 is established by PRC2 (Polycomb repressive complex 2) and represses the expression of developmental stagespecific genes (Holec and Berger, 2012).…”

“…By tagging and isolating nuclei of specific cell types in interspecific crosses, Moreno-Romero et al (2016) were recently able to examine allele-specific DNA methylation and histone modifications in Arabidopsis seeds much earlier than previous studies, at 4 d after pollination. Their findings suggest that DNA methylation is dynamic during endosperm development.…”

“…Why is methylation required for expression of the active allele? It is now clear that the hypomethylated maternal alleles of most PEGs are also preferentially modified by H3K27me3 Zhang et al, 2014;Moreno-Romero et al, 2016), which is generally correlated with repression. This suggests that DNA methylation might "protect" the paternal allele from gaining H3K27me3 (Weinhofer et al, 2010).…”

“…The sequences demethylated by DME and hypomethylated in Arabidopsis endosperm are enriched for TE remnants, often of the Helitron and Mutator types (Gehring et al, 2009;Ibarra et al, 2012;Pignatta et al, 2014, Moreno-Romero et al, 2016. The presence of TEs or their methylation status can be variable within a species (Cao et al, 2011;Schmitz et al, 2013), which has implications for imprinting stability.…”