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Imprinted expression of genes and small RNA is triggered by localized demethylation of the maternal genome in rice endosperm

ABSTRACT: We report that rice endosperm shows a specific hypomethylation of DNA in the maternal genome, preferring regions of high DNA accessibility. Maternally expressed imprinted genes are enriched for hypomethylation at putative promoter regions and transcriptional termini, and paternally expressed genes at promoters and gene bodies, mirroring our recent results in A. thaliana. However, unlike in A. thaliana, rice endosperm sRNA populations are dominated by specific strong sRNA-producing loci, and imprinted 24-nt sRNAs are expressed from both parental genomes and correlate with hypomethylation. Overlaps between imprinted sRNA loci and imprinted genes expressed from opposite alleles suggest that sRNAs may regulate genomic imprinting. Whereas sRNAs in seedling tissues primarily originate from small Class II (cut and paste) transposable elements, those in endosperm are much more uniformly derived, including sequences from other TE classes, as well as genic and intergenic regions. Our data indicate that the endosperm exhibits a unique pattern of sRNA expression and suggest that demethylation of maternal endosperm DNA is conserved in flowering plants.

ORGANISM(S): Oryza sativa

PROVIDER: GSE44898 | GEO | 2013/05/01

SECONDARY ACCESSION(S): PRJNA192671

REPOSITORIES: GEO

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Imprinted expression of genes and small RNA is triggered by localized demethylation of the maternal genome in rice endosperm

Project description:We report that rice endosperm shows a specific hypomethylation of DNA in the maternal genome, preferring regions of high DNA accessibility. Maternally expressed imprinted genes are enriched for hypomethylation at putative promoter regions and transcriptional termini, and paternally expressed genes at promoters and gene bodies, mirroring our recent results in A. thaliana. However, unlike in A. thaliana, rice endosperm sRNA populations are dominated by specific strong sRNA-producing loci, and imprinted 24-nt sRNAs are expressed from both parental genomes and correlate with hypomethylation. Overlaps between imprinted sRNA loci and imprinted genes expressed from opposite alleles suggest that sRNAs may regulate genomic imprinting. Whereas sRNAs in seedling tissues primarily originate from small Class II (cut and paste) transposable elements, those in endosperm are much more uniformly derived, including sequences from other TE classes, as well as genic and intergenic regions. Our data indicate that the endosperm exhibits a unique pattern of sRNA expression and suggest that demethylation of maternal endosperm DNA is conserved in flowering plants. Examination of DNA methylation and small RNA expression in the seeds of two cultivars from the japonica subspecies of Oryza sativa L.

2013-05-01 | E-GEOD-44898 | biostudies-arrayexpress

Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm

Project description:Imprinting describes the differential expression of alleles based upon their parent of origin. Deep sequencing of RNAs from maize endosperm and embryo tissue 14 days after pollination was used to identify imprinted genes among a set of ~12,000 genes that were expressed and contained sequence polymorphisms between the B73 and Mo17 genotypes. The analysis of parent-of-origin patterns of expression resulted in the identification of 100 putative imprinted genes in maize endosperm including 54 maternally expressed genes (MEGs) and 46 paternally expressed genes (PEGs). Three of these genes have been previously identified as imprinted while the remaining 97 genes represent novel imprinted maize genes. A genome-wide analysis of DNA methylation identified regions with reduced endosperm DNA methylation in, or near, 19 of the 100 imprinted genes. The reduced levels of DNA methylation in endosperm are caused by hypomethylation of the maternal allele for both MEGs and PEGs in all cases tested. Many of the imprinted genes with reduced DNA methylation levels also show endosperm-specific expression patterns. The imprinted maize genes were compared with imprinted genes identified in genome-wide screens of rice and Arabidopsis and at least 10 examples of conserved imprinting between maize and each of the other species were identified. Methylation profiles across endosperm tissue in B73 and Mo17 were assayed for three biological replications using a custom 2.1M gene-focused NimbleGen array.

2011-12-16 | E-GEOD-33730 | biostudies-arrayexpress

Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm

2011-12-16 | GSE33730 | GEO

A small RNA pathway mediates allelic dosage in endosperm [mRNA-seq]

Project description:Balance between maternal and paternal genomes within the triploid endosperm is necessary for normal seed development. The majority of endosperm genes are expressed in a 2:1 maternal:paternal ratio, reflecting genomic DNA content. Here we find that the 2:1 transcriptional ratio is, unexpectedly, actively regulated. In A. thaliana and A. lyrata, endosperm 24 nt small RNAs are reduced in TEs and enriched in genes compared to the embryo. We find an inverse relationship between the parent-of-origin of sRNAs and mRNAs, with genes more likely to be associated with maternally than paternally biased sRNAs. Disruption of the Pol IV sRNA pathway causes a shift toward maternal allele mRNA expression for many genes. Furthermore, paternal inheritance of an RNA Pol IV mutation is sufficient to rescue seed abortion caused by excess paternal genome dosage. Thus, RNA Pol IV mediates transcriptional balance between maternally and paternally inherited genomes in endosperm.

2017-12-15 | GSE94786 | GEO

A small RNA pathway mediates allelic dosage in endosperm [sRNA-seq]

2017-12-15 | GSE94787 | GEO

Extensive imprinted gene expression in Arabidopsis endosperm

Project description:Some flowering plant and vertebrate genes are expressed primarily or exclusively from either the maternal or paternal allele, a phenomenon called genomic imprinting. Flowering plant imprinted gene expression has been described primarily in endosperm, a terminal nutritive tissue consumed by the embryo during seed development or after germination. Imprinted expression in Arabidopsis thaliana endosperm is orchestrated by differences in cytosine DNA methylation between the paternal and maternal genomes, as well as by Polycomb group (PcG) proteins. Currently only eleven imprinted Arabidopsis genes are known. Here we use extensive sequencing of cDNA libraries to identify many new paternally and maternally imprinted genes in A. thaliana endosperm, including transcription factors, proteins involved in hormone signaling, and epigenetic regulators. The imprinted status of many maternally-expressed genes is not altered by mutations in the DNA-demethylating glycosylase DEMETER, the DNA methyltransferase MET1 or the core PcG protein FIE, indicating that these genes are regulated by novel mechanisms or deposited from maternal tissues. We did not find any imprinted genes in the embryo. Our results demonstrate that imprinted gene expression, particularly from the maternal genome, is an extensive, mechanistically complex phenomenon that likely affects multiple aspects of seed development. Epigenetics Examination of genomic imprinting in Arabidopsis endosperm

2011-03-10 | E-GEOD-24644 | biostudies-arrayexpress

Extensive imprinted gene expression in Arabidopsis endosperm

2011-03-10 | GSE24644 | GEO

Transcriptional and imprinting complexity in Arabidopsis seeds at single-nucleus resolution

Project description:Seeds are the basis of agriculture, yet their full transcriptional complexity has remained unknown. Here, we employ single-nucleus RNA-sequencing to characterize developing Arabidopsis thaliana seeds, with a focus on endosperm. Endosperm, the site of gene imprinting in plants, mediates the relationship between the maternal parent and embryo. We identify new cell types in the chalazal endosperm region, which interfaces with maternal tissue for nutrient unloading. We further demonstrate that the extent of parental bias of maternally expressed imprinted genes varies with cell cycle phase, and that imprinting of paternally expressed imprinted genes is strongest in chalazal endosperm. These data indicate imprinting in endosperm is heterogeneous and suggest that parental conflict, which is proposed to drive the evolution of imprinting, is fiercest at the boundary between filial and maternal tissues.

2021-04-06 | GSE157145 | GEO

Parental epigenetic asymmetry of PRC2-mediated histone modifications in the Arabidopsis endosperm

Project description:Parental genomes in the endosperm are marked by differential DNA methylation and are therefore epigenetically distinct. This epigenetic asymmetry is established in the gametes and maintained after fertilization by unknown mechanisms. In this manuscript, we have addressed the key question whether parentally inherited differential DNA methylation affects de novo targeting of chromatin modifiers in the early endosperm. Our data reveal that polycomb-mediated H3 lysine 27 trimethylation (H3K27me3) is preferentially localized to regions that are targeted by the DNA glycosylase DEMETER (DME), mechanistically linking DNA hypomethylation to imprinted gene expression. Our data furthermore suggest an absence of de novo DNA methylation in the early endosperm, providing an explanation how DME-mediated hypomethylation of the maternal genome is maintained after fertilization. Lastly, we show that paternal-specific H3K27me3- marked regions are located at pericentromeric regions, suggesting that H3K27me3 and DNA methylation are not necessarily exclusive marks at pericentromeric regions in the endosperm.

2016-04-26 | GSE66585 | GEO

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

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