Epigenetic signatures associated with imprinted paternally expressed genes in the Arabidopsis endosperm

Abstract

Background Imprinted genes are epigenetically modified during gametogenesis and maintain the established epigenetic signatures after fertilization, causing parental-specific gene expression. Results In 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. Conclusions The 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. Electronic supplementary material The online version of this article (10.1186/s13059-019-1652-0) contains supplementary material, which is available to authorized users.

Combinations of maternal-specific repressive epigenetic marks in the endosperm control seed dormancy

“…Our data obtained in this ( Figure 2 (Figure 2c), genes with H3K27me3/H3K9me2 but unmethylated CHG on REF6-binding sites were not significantly biased (Figure 8a, gray boxes). This data suggests that triple repressive marks are associated with paternally-biased gene expression in germinating endosperm, similar as in the developing endosperm (Moreno-Romero et al, 2019;Moreno-Romero et al, 2016). In contrast, genes with single H3K27me3 and unmethylated REF6-binding sites were significantly maternally biased (Figure 8b, upper orange boxes), supporting the idea that genes with single H3K27me3 are reactivated during germination.…”

“…Genomic imprinting leading to maternally-biased expression is predominantly connected to DNA demethylation of maternal alleles mediated by the DNA glycosylase DEMETER (Gehring et al, 2009;Hsieh et al, 2011;Park et al, 2016). In contrast, paternally-biased expression is predominantly connected to the presence of H3K27me3, H3K9me2, and CHGm on maternal alleles (Klosinska et al, 2016;Moreno-Romero et al, 2019;Moreno-Romero et al, 2016;Moreno-Romero et al, 2017). The FIS-PRC2 establishes H3K27me3 in the central cell, which is maintained on the maternal alleles after fertilization.…”

The MADS-box transcription factor PHERES1 controls imprinting in the endosperm by binding to domesticated transposons

“…P-values were determined using two-tailed Mann-Whitney tests. ( b ) Fraction of Cluster 1 and Cluster 2 binding sites that target PEGs (Figure 4—source data 1) and putative PEGs (Moreno-Romero et al, 2019). ( a, b ) H3K27me3 clusters are those defined in Figure 4b.…”

“…To determine parental gene expression ratios in 2x and 3x seeds, we used previously generated endosperm gene expression data (Martinez et al, 2018). In this dataset, L er plants were used as maternal plants pollinated with wt Col or osd1 Col plants, allowing determination of the parental origin of sequenced reads following the method described before (Moreno-Romero et al, 2019).…”

Correction to: Epigenetic signatures associated with imprinted paternally expressed genes in the Arabidopsis endosperm

“…Following publication of the original article [1], the authors reported that Additional file 4, “Table S5. Parent-of-origin RNAseq dataset of 4 DAP INTACT-purified endosperm of Col × L er reciprocal crosses” had the following error: Column 6, labeled as “Reads_Mat_Ler”, should say “Reads_pat_Col”.Column 7, labeled as “Reads_pat_Ler”, should say “Reads_mat_Ler”.…”