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Local DNA hypomethylation activates genes in rice endosperm

ABSTRACT: Cytosine methylation silences transposable elements in plants, vertebrates and fungi, but also regulates gene expression1. Plant methylation is catalyzed by three families of enzymes, each with a preferred sequence context: CG, CHG (H = A, C or T) and CHH, with CHH methylation targeted by the RNA interference (RNAi) pathway2. Arabidopsis thaliana endosperm, a placenta-like tissue that nourishes the embryo, is globally hypomethylated in the CG context while retaining high non-CG methylation3. Global methylation dynamics in seeds of cereal crops that provide the bulk of human nutrition remain unknown. Here we show that rice endosperm DNA is hypomethylated in all sequence contexts. Non-CG methylation is reduced evenly across the genome, while CG hypomethylation is localized. CHH methylation of small transposable elements is increased in embryos, suggesting that endosperm demethylation enhances transposon silencing. Genes preferentially expressed in endosperm, including those coding for major storage proteins and starch synthesizing enzymes, are frequently hypomethylated in endosperm, indicating that DNA methylation is a crucial regulator of rice endosperm biogenesis. Our data demonstrate that genome-wide reshaping of seed DNA methylation is conserved among angiosperms and has a profound effect on gene expression in cereal crops. Keywords: Epigenetics

ORGANISM(S): Oryza sativa

PROVIDER: GSE22591 | GEO | 2010/11/01

SECONDARY ACCESSION(S): PRJNA128383

REPOSITORIES: GEO

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Local DNA hypomethylation activates genes in rice endosperm

Project description:Cytosine methylation silences transposable elements in plants, vertebrates and fungi, but also regulates gene expression1. Plant methylation is catalyzed by three families of enzymes, each with a preferred sequence context: CG, CHG (H = A, C or T) and CHH, with CHH methylation targeted by the RNA interference (RNAi) pathway2. Arabidopsis thaliana endosperm, a placenta-like tissue that nourishes the embryo, is globally hypomethylated in the CG context while retaining high non-CG methylation3. Global methylation dynamics in seeds of cereal crops that provide the bulk of human nutrition remain unknown. Here we show that rice endosperm DNA is hypomethylated in all sequence contexts. Non-CG methylation is reduced evenly across the genome, while CG hypomethylation is localized. CHH methylation of small transposable elements is increased in embryos, suggesting that endosperm demethylation enhances transposon silencing. Genes preferentially expressed in endosperm, including those coding for major storage proteins and starch synthesizing enzymes, are frequently hypomethylated in endosperm, indicating that DNA methylation is a crucial regulator of rice endosperm biogenesis. Our data demonstrate that genome-wide reshaping of seed DNA methylation is conserved among angiosperms and has a profound effect on gene expression in cereal crops. Keywords: Epigenetics Examination of DNA methylation in rice

2010-11-01 | E-GEOD-22591 | biostudies-arrayexpress

Genome-wide demethylation of Arabidopsis endosperm

Project description:Parent-of-origin-specific (imprinted) gene expression is regulated in Arabidopsis thaliana endosperm by cytosine demethylation of the maternal genome mediated by the DNA glycosylase DEMETER, but the extent of the methylation changes is not known. Here we show that virtually the entire endosperm genome is demethylated, coupled with extensive local non-CG hypermethylation of siRNA-targeted sequences. Mutation of DEMETER partially restores endosperm CG methylation to levels found in other tissues, indicating that CG demethylation is specific to maternal sequences. Endosperm demethylation is accompanied by CHH hypermethylation of embryo transposable elements. Our findings demonstrate extensive reconfiguration of the endosperm methylation landscape that likely reinforces transposon silencing in the embryo. Keywords: Epigenetics; bisulfite sequencing Examination of DNA methylation in four Arabidopsis tissues Description of processed data and raw data file contents can be found in the attached README.txt file

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Genome-wide demethylation of Arabidopsis endosperm

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Extensive demethylation of repetitive elements during seed development underlies gene imprinting

Project description:DNA methylation is an epigenetic mark associated with transposable element silencing and gene imprinting in flowering plants and mammals. In plants, imprinting occurs in the endosperm, which nourishes the embryo during seed development. We have profiled Arabidopsis DNA methylation genome-wide in the embryo and endosperm. Large-scale methylation changes accompany endosperm development and endosperm-specific gene expression. Transposable element fragments are extensively demethylated in the endosperm. We discovered new imprinted genes by identifying candidate genes associated with the top differentially methylated regions. Our data suggest that imprinting in plants evolved from genome defense against transposable elements. Keywords: Affinity-purification on microarray

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DNA methylation dynamics during early plant life

Project description:We uncover distinct DNA methylation dynamics over genes and repeat sequences during early plant life in Arabidopsis. While gene body methylation, which is restricted to CG sites and concerns 20-30% of all genes is detected at all stages examined, it typically fluctuates over a few CGs, with no coherent pattern. In contrast, transposable elements and their relics as well as other repeat sequences, have consistently high methylation levels at CGs and show increasing CHG and especially CHH methylation during embryogenesis. Remarkably, methylation reaches 100% at many individual CHH sites in the mature embryo, compared to the 10-20% methylation usually observed at CHH sites in seedlings or adult plants. Moreover, the progressive increase in CHG and CHH methylation in embryos mirrors the loss of DNA methylation at CG and CHG sites in the endosperm, suggesting transfer of information from the endosperm to the embryo, presumably in the form of small RNAs. Finally, impairing the embryo to seedling transition through loss of PRC2 activity results in the persistence of high CHH methylation levels after germination and specifically over sequences that are targeted by the RNA-directed DNA methylation (RdDM) machinery. Collectively, our findings indicate a lack of extensive resetting of DNA methylation patterns during early plant life and point instead to an important role of RdDM in targeting DNA methylation to transposable element and other repeat sequences in all cells of the mature embryo.

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Extensive demethylation of repetitive elements during seed development underlies gene imprinting

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The ortholog of DDM1 is mainly required for CHG and CG methylation of heterochromatin and is involved in DRM2-mediated CHH methylation that targets mostly genic regions of the rice genome

Project description:OsDDM1 and OsDRM2 display functional specificities that define distinct DNA methylation pathways in the bulk of DNA methylation of the rice genome Cr_DJ.CG.bw: Cr_DJ CG methylation Cr_DJ.CHG.bw: Cr_DJ CHG methylation Cr_DJ.CHH.bw: Cr_DJ CHH methylation ddm1ab.CG.bw: ddm1a/1b CG methylation ddm1ab.CHG.bw: ddm1a/1b CHG methylation ddm1ab.CHH.bw: ddm1a/1b CHH methylation S706.CG.bw: osdrm2 CG methylation S706.CHG.bw: osdrm2 CHG methylation S706.CHH.bw: osdrm2 CHH methylation H3k9me2_macs_peaks.xls: CrDJ H3K9me2 modification peaks H3k9me2_macs_treat_afterfiting.wig: CrDJ H3K9me2 modification wig CrDJ_K27_macs_peaks.xls: CrDJ H3K27me3 modification peaks CrDJ_K27_macs_treat_afterfiting.wig: CrDJ H3K27me3 modification wig DJvsddm1a1b_DESeq2_treated_results.xls: CrDJ and osddm1a1b different expression genes DJvsS706_DEseq2_treated.results.xls: CrDJ and osdrm2 different expression genes smRNA24nt.gff: CrDJ 24nt smRNA smRNA24nt.706.gff: osdrm2 24nt smRNA

2016-06-13 | E-GEOD-81436 | biostudies-arrayexpress

Control of Rice Tillering by RNA-directed DNA Methylation at Miniature Inverted-repeat Transposable Elements

Project description:In rice, tillering is an important agricultural trait that affects plant architecture and grain yield. RNA-directed DNA methylation (RdDM), which establishes DNA methylation in all CG, CHG and CHH sequence contexts and maintains CHH methylation in plants, silences transposable elements (TEs) and regulates gene expression. Here we report that knockdown and knockout of OsNRPD1a and OsNRPD1b, genes encoding two orthologues of the largest subunit of OsPol IV holoenzyme that transcribes 24-nucleotide (nt) siRNAs in RdDM, lead to a high-tillering phenotype, in addition to dwarfism and smaller panicles. In the shoot base of the osnrpd1a/b RNAi line, many genes are dysregulated, due to loss of 24-nt siRNAs and CHH methylation. Among these genes, OsMIR156d and OsMIR156j, which promote rice tillering, is derepressed when CHH methylation at Miniature Inverted-Repeat Transposable Elements (MITEs) in the promoters of OsMIR156d and OsMIR156j is lost. By contrast, D14, which suppresses rice tillering, is repressed when CHH methylation at a MITE in the 3’UTR of D14 is lost. Deletion of the MITE that is targeted by RdDM in D14 is sufficient to cause high-tillering. Our findings reveal control of rice tillering by RdDM at MITEs and provide the potential targets for agronomic trait enhancement by epigenome editing.

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Both maternally and paternally imprinted genes regulate seed development in rice

Project description:Genetic imprinting is an epigenetic phenomenon that describes unequal expression of paternal and maternal alleles of a gene in sexually reproducing organisms including mammals and flowering plants. The function of imprinted genes was rarely reported. We report genome-wide analysis of gene expression, DNA methylation, and small RNAs in the rice endosperm and functional tests of five imprinted genes in seed development using CRISPR/Cas9 editing technology. We identified 162 maternally expressed genes(MEGs) and 95 paternally expressed genes (PEGs) in the rice endosperm, which were associated with miniature inverted-repeat transposable elements, imprinted differentially methylated loci, and some 21-22-siRNAs and lncRNAs. Remarkably, one-third of MEGs and nearly half of PEGs were associated with grain-yield quantitative trait loci and enriched in the endosperm-expressed genes. Disrupting two MEGs increased the amount of small starch granules and reduced grain size, weight, and embryo size, while mutating three PEGs reduced starch content and seed fertility. Our data support both MEGs and PEGs in rice are required for starch and nutrient accumulation, mediating offspring fitness and optimal seed size. This imprinting strategy provides potential means for improving grain yield of rice and other cereal crops.

2017-02-04 | GSE77710 | GEO

Rice interploidy crosses disrupt epigenetic regulation, gene expression, and seed development

Project description:Seed development in angiosperms requires a 2:1 maternal-to-paternal genome ratio (2m:1p) in the endosperm. When the ratio is disrupted, the seed development is impaired. Rice interploidy crosses result in endosperm failures. Here we report that the defective endosperm was associated with nonadditive expression of small RNAs and protein-coding genes. Interestingly, 24-nt siRNAs were enriched in the 5’ and 3’ flanking sequences of nonadditively expressed genes in the interploidy crosses and negatively associated with the expression of imprinted genes. Furthermore, some PRC2 gene family members and the genes for DNA methylation including OsMET1b and OsCMT3a were upregulated in the 2X4 cross but repressed in the reciprocal cross. These different epigenetic effects could lead to precocious or delayed cellularization during endosperm development. Notably, many endosperm-preferred genes including starch metabolic and storage protein genes during grain filling were associated with DNA methylation or H3K27me3 and repressed in both 2X4 and 4X2 crosses. WUSCHEL homeobox2 (WOX2)-like (WOX2L), an endosperm-preferred gene, was expressed specifically in the rice endosperm, on contrary to WOX2 expression in the Arabidopsis embryo. CRISPR/Cas9 editing of WOX2L in transgenic rice blocked starch and protein accumulation, resulting in seed abortion. In addition to gene repression, disrupting epigenetic process in the interploidy crosses also induced expression of stress-responsive genes. Thus, maintaining the 2m:1p genome ratio in the endosperm is essential for normal grain development in rice and other cereal crops.

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