Miniature Inverted-Repeat Transposable Elements (MITEs) Have Been Accumulated through Amplification Bursts and Play Important Roles in Gene Expression and Species Diversity in Oryza sativa

Chen, Lu; Chen, Jiongjiong; Yu, Zhang; Hu, Qun; Su, Wenqing; Kuang, Hanhui

doi:10.1093/molbev/msr282

Cited by 195 publications

(209 citation statements)

References 65 publications

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“…5B). This group is largely comprised of miniature inverted-repeat TEs (MITEs), which preferentially occur near genes in euchromatic regions and are the predominant target of CHH methylation in rice tissues (16,23). In contrast, 24-nt sRNA production in endosperm is much more evenly distributed across different TE classes and sizes (Fig.…”

Section: Differentially Methylated Regions Are Enriched Around and Wimentioning

confidence: 99%

Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm

Rodrigues

Ruan

Nishimura

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

132

184

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Arabidopsis thaliana endosperm, a transient tissue that nourishes the embryo, exhibits extensive localized DNA demethylation on maternally inherited chromosomes. Demethylation mediates parent-of-origin-specific (imprinted) gene expression but is apparently unnecessary for the extensive accumulation of maternally biased small RNA (sRNA) molecules detected in seeds. Endosperm DNA in the distantly related monocots rice and maize is likewise locally hypomethylated, but whether this hypomethylation is generally parent-of-origin specific is unknown. Imprinted expression of sRNA also remains uninvestigated in monocot seeds. Here, we report high-coverage sequencing of the Kitaake rice cultivar that enabled us to show that localized hypomethylation in rice endosperm occurs solely on 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 more uniformly derived, including sequences from other transposon classes, as well as genic and intergenic regions. Our data indicate that the endosperm exhibits a unique pattern of sRNA expression and suggest that localized hypomethylation of maternal endosperm DNA is conserved in flowering plants.D NA methylation is a covalent modification of cytosine observed across the tree of life (1). In plants, methylation is mediated by distinct enzymatic systems in the CG, CHG, and CHH contexts (where H is A, C, or T), and regulates gene expression and transposon repression (2). The establishment of plant DNA methylation in all sequence contexts and the maintenance of CHH methylation is mediated by a specialized branch of the RNA interference pathway that generates nuclear-targeted 24-nt small RNA (sRNA) molecules (3, 4). Plants also possess DEMETER (DME) family DNA glycosylases that actively demethylate DNA by excising 5-methylcytosine in all sequence contexts (5, 6), with a preference for relatively euchromatic transposable elements (TEs) (7).Homologs of DME are expressed in various tissues of the model dicot Arabidopsis thaliana throughout development (8), but DME expression is most prominent in the so-called gamete companion cells: the central and vegetative cells (9, 10). The vegetative cell forms the pollen tube that delivers two sperm cells, one of which fuses with the haploid egg cell to form the embryo, whereas the other fuses with the adjacent diploid centra...

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Section: Differentially Methylated Regions Are Enriched Around and Wimentioning

confidence: 99%

Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm

Rodrigues

Ruan

Nishimura

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

132

184

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“…In contrast to the more localized pattern of repeats close to centromeres in Arabidopsis, repeats in rice are widely spread on the chromosomes. In addition, the rice genome contains a large number of miniature inverted-repeat transposable elements (MITEs), a majority of which are associated with genes (Feschotte and Wessler, 2002;Lu et al, 2012). Extensive genome-wide DNA methylation and histone modification data sets have been generated in rice (Feng et al, 2010;He et al, 2010;Zemach et al, 2010;Liu et al, 2015).…”

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confidence: 99%

Analysis of Chromatin Regulators Reveals Specific Features of Rice DNA Methylation Pathways

Tan

Zhou²,

Zhou³

et al. 2016

Plant Physiol.

115

157

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Plant DNA methylation that occurs at CG, CHG, and CHH sites (H = A, C, or T) is a hallmark of the repression of repetitive sequences and transposable elements (TEs). The rice (Oryza sativa) genome contains about 40% repetitive sequence and TEs and displays specific patterns of genome-wide DNA methylation. The mechanism responsible for the specific methylation patterns is unclear. Here, we analyzed the function of OsDDM1 (Deficient in DNA Methylation 1) and OsDRM2 (Deficient in DNA Methylation 1) in genome-wide DNA methylation, TE repression, small RNA accumulation, and gene expression. We show that OsDDM1 is essential for high levels of methylation at CHG and, to a lesser extent, CG sites in heterochromatic regions and also is required for CHH methylation that mainly locates in the genic regions of the genome. In addition to a large member of TEs, loss of OsDDM1 leads to hypomethylation and up-regulation of many protein-coding genes, producing very severe growth phenotypes at the initial generation. Importantly, we show that OsDRM2 mutation results in a nearly complete loss of CHH methylation and derepression of mainly small TE-associated genes and that OsDDM1 is involved in facilitating OsDRM2-mediated CHH methylation. Thus, the function of OsDDM1 and OsDRM2 defines distinct DNA methylation pathways in the bulk of DNA methylation of the genome, which is possibly related to the dispersed heterochromatin across chromosomes in rice and suggests that DNA methylation mechanisms may vary among different plant species.DNA methylation in flowering plants occurs in three sequence contexts: the so-called symmetric CG and CHG and the asymmetric CHH, where H is any nucleotide except G. Methylation in each context is believed to be catalyzed primarily by a specific family of DNA methyltransferases: MET1 (homologous to animal Dnmt1) for CG, plant-specific chromomethylases (CMT3 and CMT2) for CHG, and DRM2 (homologous to animal Dnmt3) for CHH (Law and Jacobsen, 2010).Recently, it was shown that CMT2 is a major CHH methyltransferase in Arabidopsis (Arabidopsis thaliana; Zemach et al., 2013;Stroud et al., 2014). The majority of plant methylation is found in transposable elements (TEs) and transcribed TE genes (known as transposable element-related genes [TEGs]) and is crucial for the repression of TE expression and transposition (Law and Jacobsen, 2010). Substantial methylation also is found in the bodies of active genes, where methylation is generally restricted to the CG context (Law and Jacobsen, 2010;Zemach et al., 2010). Methylation in all sequence contexts also is found in the promoter regions of many genes, which represses gene expression.In Arabidopsis, the maintenance of CHH methylation is mediated by RNA-directed DNA methylation (RdDM) involving the methyltransferase activity of DRM2 (Law and Jacobsen, 2010). DNA methylation also is influenced by chromatin factors. For instance, the Arabidopsis Snf2 family nucleosome remodeler DDM1, which can shift nucleosomes in vitro (Brzeski and Jerzmanowski, 2003), is essential fo...

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“…In general, TEs associated with heterochromatin accumulate at pericentromeric regions of chromosomes 13,14 , whereas a substantial number of TEs are also found within gene units, particularly in introns 8,15,16 . Despite their abundance, however, epigenetic regulation of intragenic TEs and their impact on modes of transcription remain largely unexplored.…”

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confidence: 99%

Mechanism for full-length RNA processing of Arabidopsis genes containing intragenic heterochromatin

et al. 2013

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Genomes of higher eukaryotes contain many transposable elements, which often localize within the transcribed regions of active genes. Although intragenic transposable elements can be silenced to form heterochromatin, the impact of intragenic heterochromatin on transcription and RNA processing remains largely unexplored. Here we show using a flowering plant, Arabidopsis, that full-length transcript formation over intragenic heterochromatin depends on a protein named IBM2 (Increase in Bonsai Methylation 2), which has a Bromo-Adjacent Homology domain and an RNA recognition motif. Mutation of ibm2 triggers premature termination of transcripts with 3 0 RNA processing around intragenic heterochromatin at loci including the H3K9 demethylase gene IBM1. The need for IBM2 is circumvented in variant alleles that lack the heterochromatic domain. Our results reveal a mechanism that masks deleterious effects of intragenic heterochromatin, providing evolutionary sources for genetic and epigenetic variations.

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Miniature Inverted-Repeat Transposable Elements (MITEs) Have Been Accumulated through Amplification Bursts and Play Important Roles in Gene Expression and Species Diversity in Oryza sativa

Cited by 195 publications

References 65 publications

Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm

Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm

Analysis of Chromatin Regulators Reveals Specific Features of Rice DNA Methylation Pathways

Mechanism for full-length RNA processing of Arabidopsis genes containing intragenic heterochromatin

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