Genome-wide high resolution parental-specific DNA and histone methylation maps uncover patterns of imprinting regulation in maize

Abstract

Genetic imprinting is a specific epigenetic phenomenon in which a subset of genes is expressed depending on their parentof-origin. Two types of chromatin modifications, DNA methylation and histone modification, are generally believed to be involved in the regulation of imprinting. However, the genome-wide correlation between allele-specific chromatin modifications and imprinted gene expression in maize remains elusive. Here we report genome-wide high resolution allelespecific maps of DNA methylation and histone H3 lysine 27 trimethylation (H3K27me3) in maize endosperm. For DNA methylation, thousands of parent-of-origin dependent differentially methylated regions (pDMRs) were identified. All pDMRs were uniformly paternally hypermethylated and maternally hypomethylated. We also identified 1131 allele-specific H3K27me3 peaks that are preferentially present in the maternal alleles. Maternally expressed imprinted genes (MEGs) and paternally expressed imprinted genes (PEGs) had different patterns of allele-specific DNA methylation and H3K27me3. Allele-specific expression of MEGs was not directly related to allele-specific H3K27me3, and only a subset of MEGs was associated with maternal-specific DNA demethylation, which was primarily located in the upstream and 59 portion of gene body regions. In contrast, allele-specific expression of a majority of PEGs was related to maternal-specific H3K27me3, with a subgroup of PEGs also associated with maternal-specific DNA demethylation. Both pDMRs and maternal H3K27me3 peaks associated with PEGs are enriched in gene body regions. Our results indicate highly complex patterns of regulation on genetic imprinting in maize endosperm.

Genomic DNA methylation analyses reveal the distinct profiles in castor bean seeds with persistent endosperms

“…These observations show that CG and CHG methylation are more effectively maintained in short TEs than CHH methylation during DNA replication, while CHH methylation is more randomly distributed across short and long TEs, with a relatively low level of methylation compared with CG and CHG in both embryo and endosperm. Compared with previously studied plants such as Arabidopsis (Hsieh et al, 2009), rice (Zemach et al, 2010a), maize (Zhang et al, 2014;Lu et al, 2015), and soybean (Glycine max; Song et al, 2013), the genomic methylation profiles in castor bean seem to be distinct.…”

“…3A). Compared with the genomic DNA methylation levels in Arabidopsis (Hsieh et al, 2009), rice (Zemach et al, 2010a), and maize (Zhang et al, 2014;Lu et al, 2015), we found that the genomic DNA hypomethylation of endosperm tissues relative to embryo tissues was extensive in angiosperms, particularly for dicotyledons ( Fig. 3A), although the biological roles of endosperm hypomethylation remain unknown.…”

“…In particular, DNA methylation was considered as a major regulator of gene imprinting that mainly manifests itself in the endosperm of angiosperm plants, closely associated with endosperm and seed development, such as the imprinted genes MEA (Grossniklaus et al, 1998;Köhler et al, 2003), FWA (Kinoshita et al, 2004), and FIS2 (Jullien et al, 2006). Investigations of genomic DNA methylation in the seeds of Arabidopsis (Gehring et al, 2009;Hsieh et al, 2009), rice (Oryza sativa; Zemach et al, 2010a), and maize (Zea mays; Zhang et al, 2014;Lu et al, 2015) revealed extensive hypomethylation in the endosperm genome. However, the mechanism of how the extent and pattern of DNA methylation are established and whether the extent and pattern of DNA methylation are conserved in plant seeds is largely unclear.…”

Genomic Analysis of the DNA Replication Timing Program during Mitotic S Phase in Maize (Zea mays) Root Tips

“…H3K56ac has roles in several different biological processes, including transcription, DNA replication and repair, and nucleosome dynamics in yeast and other eukaryotes (Masumoto et al, 2005;Xu et al, 2005;Han et al, 2007;Kaplan et al, 2008;Williams et al, 2008). H3K27me3 is a mark for facultative heterochromatin and is associated with repressed transcription, developmental gene regulation, and imprinting in maize (Wang et al, 2009;Makarevitch et al, 2013;Zhang et al, 2014). We expected H3K4me3 and H3K56ac to mark open chromatin in the euchromatic portion of the genome and H3K27me3 to mark chromatin that is more condensed, though not as tightly packaged as constitutive heterochromatin.…”

Epigenetics: from the past to the present

“…siRNA are involved in the formation of heterochromatin in the centromeres of Schizosaccharomyces pombe. In plants, they are involved in RNA-directed DNA methylation (RdDM) (Lejeune & Allshire 2011;Zhang et al 2014).…”