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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 parent-of-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 allele-specific 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 5' 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.

SUBMITTER: Zhang M

PROVIDER: S-EPMC3875858 | biostudies-literature | 2014 Jan

REPOSITORIES: biostudies-literature

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

Zhang Mei M Xie Shaojun S Dong Xiaomei X Zhao Xin X Zeng Biao B Chen Jian J Li Hui H Yang Weilong W Zhao Hainan H Wang Gaokui G Chen Zongliang Z Sun Silong S Hauck Andrew A Jin Weiwei W Lai Jinsheng J

Genome research 20131016 1

Genetic imprinting is a specific epigenetic phenomenon in which a subset of genes is expressed depending on their parent-of-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 allele-specific maps of DNA methy ...[more]

PMID: 24131563

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Project description:BackgroundGenome-wide DNA methylation at a single nucleotide resolution in different primary cells of the mammalian genome helps to determine the characteristics and functions of tissue-specific hypomethylated regions (TS-HMRs). We determined genome-wide cytosine methylation maps at 91X and 36X coverage of newborn female mouse primary dermal fibroblasts and keratinocytes and compared with mRNA-seq gene expression data.ResultsThese high coverage methylation maps were used to identify HMRs in both cell types. A total of 2.91% of the genome are in keratinocyte HMRs, and 2.15% of the genome are in fibroblast HMRs with 1.75% being common. Half of the TS-HMRs are extensions of common HMRs, and the remaining are unique TS-HMRs. Four levels of CG methylation are observed: 1) total unmethylation for CG dinucleotides in HMRs in CGIs that are active in all tissues; 2) 10% to 40% methylation for TS-HMRs; 3) 60% methylation for TS-HMRs in cells types where they are not in HMRs; and 4) 70% methylation for the nonfunctioning part of the genome. SINE elements are depleted inside the TS-HMRs, while highly enriched in the surrounding regions. Hypomethylation at the last exon shows gene repression, while demethylation toward the gene body positively correlates with gene expression. The overlapping HMRs have a more complex relationship with gene expression. The common HMRs and TS-HMRs are each enriched for distinct Transcription Factor Binding Sites (TFBS). C/EBPβ binds to methylated regions outside of HMRs while CTCF prefers to bind in HMRs, highlighting these two parts of the genome and their potential interactions.ConclusionsKeratinocytes and fibroblasts are of epithelial and mesenchymal origin. High-resolution methylation maps in these two cell types can be used as reference methylomes for analyzing epigenetic mechanisms in several diseases including cancer. Please see related article at the following link: http://www.epigeneticsandchromatin.com/content/7/1/34.

Project description:BackgroundEpigenetic modifications play important roles in plant and animal development. DNA methylation impacts the transposable element (TE) silencing, gene imprinting and expression regulation.ResultsThrough a genome-wide analysis, DNA methylation peaks were characterized and mapped in maize embryo and endosperm genome, respectively. Distinct methylation level was observed across maize embryo and endosperm. The maize embryo genome contained more DNA methylation than endosperm. Totally, 985,478 CG islands (CGIs) were identified and most of them were unmethylated. More CGI shores were methylated than CGIs in maize suggested that DNA methylation level was not positively correlated with CpG density. The promoter sequence and transcriptional termination region (TTR) were more methylated than the gene body (intron and exon) region based on peak number and methylated depth. Result showed that 99% TEs were methylated in maize embryo, but a large portion of them (34.8%) were not methylated in endosperm. Maize embryo and endosperm exhibit distinct pattern/level of methylation. The most differentially methylated region between embryo and endosperm are CGI shores. Our results indicated that DNA methylation is associated with both gene silencing and gene activation in maize. Many genes involved in embryogenesis and seed development were found differentially methylated in embryo and endosperm. We found 41.5% imprinting genes were similarly methylated and 58.5% imprinting genes were differentially methylated between embryo and endosperm. Methylation level was associated with allelic silencing of only a small number of imprinting genes. The expression of maize DEMETER-like (DME-like) gene and MBD101 gene (MBD4 homolog) were higher in endosperm than in embryo. These two genes may be associated with distinct methylation levels across maize embryo and endosperm.ConclusionsThrough MeDIP-seq we systematically analyzed the methylomes of maize embryo and endosperm and results indicated that the global methylation status of embryo was more than that of the endosperm. Differences could be observed at the total number of methylation peaks, DMRs and specific methylated genes which were tightly associated with development of embryo and endosperm. Our results also revealed that many DNA methylation regions didn't affect transcription of the corresponding genes.

Dataset Information

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

Publications

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

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