Abstract
BackgroundImprinted genes are epigenetically modified during gametogenesis and maintain the established epigenetic signatures after fertilization, causing parental-specific gene expression.ResultsIn this study, we show that imprinted paternally expressed genes (PEGs) in the Arabidopsis endosperm are marked by an epigenetic signature of Polycomb Repressive Complex2 (PRC2)-mediated H3K27me3 together with heterochromatic H3K9me2 and CHG methylation, which specifically mark the silenced maternal alleles of PEGs. The co-occurrence of H3K27me3 and H3K9me2 on defined loci in the endosperm drastically differs from the strict separation of both pathways in vegetative tissues, revealing tissue-specific employment of repressive epigenetic pathways in plants. Based on the presence of this epigenetic signature on maternal alleles, we are able to predict known PEGs at high accuracy and identify several new PEGs that we confirm using INTACT-based transcriptomes generated in this study.ConclusionsThe presence of the three repressive epigenetic marks, H3K27me3, H3K9me2, and CHG methylation on the maternal alleles in the endosperm serves as a specific epigenetic signature that allows prediction of genes with parental-specific gene expression. Our study reveals that there are substantially more PEGs than previously identified, indicating that paternal-specific gene expression is of higher functional relevance than currently estimated. The combined activity of PRC2-mediated H3K27me3 together with the heterochromatic H3K9me3 has also been reported to silence the maternal Xist locus in mammalian preimplantation embryos, suggesting convergent employment of both pathways during the evolution of genomic imprinting.
Highlights
Imprinted genes are epigenetically modified during gametogenesis and maintain the established epigenetic signatures after fertilization, causing parental-specific gene expression
The maternal alleles of paternally expressed genes (PEGs) are marked by H3K27me3, H3K9me2, and CHG methylation In a previous study, we revealed that H3K27me3 and H3K9me2 overlapped in the endosperm at pericentromeric heterochromatic regions of the paternal genome, suggesting a partial functional redundancy of both modifications [8]
We found that about one third of genes marked by H3K27me3 on the maternal alleles were marked by H3K9me2 (Fig. 1a, hypergeometric test, P = 0 (Col × Ler crosses); Additional file 1: Figure S1A, P = 0 (Ler × Col crosses))
Summary
Imprinted genes are epigenetically modified during gametogenesis and maintain the established epigenetic signatures after fertilization, causing parental-specific gene expression. Repression of the maternal alleles of PEGs is mediated by the activity of the FIS-PRC2 [12], consistent with maternal PEG alleles being marked by H3K27me3 [8] In this manuscript, we addressed the mechanism of maternal allele repression in PEGs. We surprisingly found that PEGs are regulated by two otherwise largely exclusive epigenetic repressive pathways, the FIS2-PRC2 and the pathway establishing the heterochromatin-localized H3K9me modification [13]. We surprisingly found that PEGs are regulated by two otherwise largely exclusive epigenetic repressive pathways, the FIS2-PRC2 and the pathway establishing the heterochromatin-localized H3K9me modification [13] We demonstrate that both modifications, H3K27me and H3K9me, overlap on the maternal alleles of the majority of PEGs. Our data suggest that most likely FIS-PRC2 acts first and is required to establish H3K9me.
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