scholarly journals Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Jaemyung Choi ◽  
David B Lyons ◽  
Daniel Zilberman
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Small Rna ◽  
Histone H3 ◽  
Histone H1 ◽  
Dna Methyltransferases ◽  
Flowering Plants ◽  
Genomic Sequences ◽  
Rna Molecules ◽  
Rna Biogenesis

Flowering plants utilize small RNA molecules to guide DNA methyltransferases to genomic sequences. This RNA-directed DNA methylation (RdDM) pathway preferentially targets euchromatic transposable elements. However, RdDM is thought to be recruited by methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin. How RdDM is targeted to euchromatin despite an affinity for H3K9me is unclear. Here we show that loss of histone H1 enhances heterochromatic RdDM, preferentially at nucleosome linker DNA. Surprisingly, this does not require SHH1, the RdDM component that binds H3K9me. Furthermore, H3K9me is dispensable for RdDM, as is CG DNA methylation. Instead, we find that non-CG methylation is specifically associated with small RNA biogenesis, and without H1 small RNA production quantitatively expands to non-CG methylated loci. Our results demonstrate that H1 enforces the separation of euchromatic and heterochromatic DNA methylation pathways by excluding the small RNA-generating branch of RdDM from non-CG methylated heterochromatin.

scholarly journals Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin

2021 ◽  
Author(s):  
Jaemyung Choi ◽  
David Bruce Lyons ◽  
Daniel Zilberman
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Small Rna ◽  
Histone H3 ◽  
Histone H1 ◽  
Dna Methyltransferases ◽  
Flowering Plants ◽  
Genomic Sequences ◽  
Rna Molecules ◽  
Rna Biogenesis

Flowering plants utilize small RNA molecules to guide DNA methyltransferases to genomic sequences. This RNA-directed DNA methylation (RdDM) pathway preferentially targets euchromatic transposable elements. However, RdDM is thought to be recruited by methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin. How RdDM is targeted to euchromatin despite an affinity for H3K9me is unclear. Here we show that loss of histone H1 enhances heterochromatic RdDM, preferentially at nucleosome linker DNA. Surprisingly, this does not require SHH1, the RdDM component that binds H3K9me. Furthermore, H3K9me is dispensable for RdDM, as is CG DNA methylation. Instead, we find that non-CG methylation is specifically required for small RNA biogenesis, and without H1 small RNA production quantitatively expands to non-CG methylated loci. Our results demonstrate that H1 enforces the separation of euchromatic and heterochromatic DNA methylation pathways by excluding the small RNA-generating branch of RdDM from non-CG methylated heterochromatin.

scholarly journals Loss of mCHH islands in maize chromomethylase and DDM1-type nucleosome remodeler mutants

2018 ◽  
Author(s):  
Fang-Fang Fu ◽  
R. Kelly Dawe ◽  
Jonathan I. Gent
Keyword(s):  
Dna Methylation ◽  
Small Rna ◽  
Double Mutant ◽  
Histone H3 ◽  
Dna Methyltransferases ◽  
Plant Tissues ◽  
Rna Expression ◽  
Nucleosome Remodeling ◽  
Genes Encoding

ABSTRACTPlants make use of three types of DNA methylation, each characterized by distinct DNA methyltransferases. One type, RNA-directed DNA methylation (RdDM), is guided by siRNAs to the edges of transposons that are close to genes, areas called mCHH islands in maize. Another type, chromomethylation, is guided by histone H3 lysine 9 methylation to heterochromatin across the genome. We examined DNA methylation and small RNA expression in plant tissues that were mutant for both copies of the genes encoding chromomethylases as well as mutants for both copies of the genes encoding DDM1-type nucleosome remodelers, which facilitate chromomethylation. Both sets of double mutants were nonviable but produced embryos and endosperm. RdDM was severely compromised in the double mutant embryos, both in terms of DNA methylation and siRNAs. Loss of 24nt siRNA from mCHH islands was coupled with a gain of 21, 22, and 24nt siRNAs in heterochromatin. These results reveal a requirement for both chromomethylation and DDM1-type nucleosome remodeling for RdDM in mCHH islands, which we hypothesize is due to dilution of RdDM components across the genome when heterochromatin is compromised.

scholarly journals Interplay between Histone and DNA Methylation Seen through Comparative Methylomes in Rare Mendelian Disorders

2021 ◽  
Vol 22 (7) ◽  
pp. 3735
Author(s):  
Guillaume Velasco ◽  
Damien Ulveling ◽  
Sophie Rondeau ◽  
Pauline Marzin ◽  
Motoko Unoki ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Catalytic Domain ◽  
De Novo ◽  
Mutation Screening ◽  
Histone H3 ◽  
Regulatory Elements ◽  
Germline Mutations ◽  
Dna Methyltransferases ◽  
Mendelian Disorders ◽  
Epigenetic Machinery

DNA methylation (DNAme) profiling is used to establish specific biomarkers to improve the diagnosis of patients with inherited neurodevelopmental disorders and to guide mutation screening. In the specific case of mendelian disorders of the epigenetic machinery, it also provides the basis to infer mechanistic aspects with regard to DNAme determinants and interplay between histone and DNAme that apply to humans. Here, we present comparative methylomes from patients with mutations in the de novo DNA methyltransferases DNMT3A and DNMT3B, in their catalytic domain or their N-terminal parts involved in reading histone methylation, or in histone H3 lysine (K) methylases NSD1 or SETD2 (H3 K36) or KMT2D/MLL2 (H3 K4). We provide disease-specific DNAme signatures and document the distinct consequences of mutations in enzymes with very similar or intertwined functions, including at repeated sequences and imprinted loci. We found that KMT2D and SETD2 germline mutations have little impact on DNAme profiles. In contrast, the overlapping DNAme alterations downstream of NSD1 or DNMT3 mutations underlines functional links, more specifically between NSD1 and DNMT3B at heterochromatin regions or DNMT3A at regulatory elements. Together, these data indicate certain discrepancy with the mechanisms described in animal models or the existence of redundant or complementary functions unforeseen in humans.

scholarly journals The histone variant H2A.W and linker histone H1 co-regulate heterochromatin accessibility and DNA methylation

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Pierre Bourguet ◽  
Colette L. Picard ◽  
Ramesh Yelagandula ◽  
Thierry Pélissier ◽  
Zdravko J. Lorković ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Histone H1 ◽  
Epigenetic Modifications ◽  
Flowering Plants ◽  
Linker Histone ◽  
Histone Variant ◽  
Null Mutant ◽  
Chromatin Compaction ◽  
Linker Histone H1

AbstractIn flowering plants, heterochromatin is demarcated by the histone variant H2A.W, elevated levels of the linker histone H1, and specific epigenetic modifications, such as high levels of DNA methylation at both CG and non-CG sites. How H2A.W regulates heterochromatin organization and interacts with other heterochromatic features is unclear. Here, we create a h2a.w null mutant via CRISPR-Cas9, h2a.w-2, to analyze the in vivo function of H2A.W. We find that H2A.W antagonizes deposition of H1 at heterochromatin and that non-CG methylation and accessibility are moderately decreased in h2a.w-2 heterochromatin. Compared to H1 loss alone, combined loss of H1 and H2A.W greatly increases accessibility and facilitates non-CG DNA methylation in heterochromatin, suggesting co-regulation of heterochromatic features by H2A.W and H1. Our results suggest that H2A.W helps maintain optimal heterochromatin accessibility and DNA methylation by promoting chromatin compaction together with H1, while also inhibiting excessive H1 incorporation.

scholarly journals Genome-wide characterization of DNA methylation, small RNA expression, and histone H3 lysine nine di-methylation in Brassica rapa L.

DNA Research ◽  
2018 ◽  
Vol 25 (5) ◽  
pp. 511-520 ◽  
Author(s):  
Satoshi Takahashi ◽  
Kenji Osabe ◽  
Naoki Fukushima ◽  
Shohei Takuno ◽  
Naomi Miyaji ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Brassica Rapa ◽  
Small Rna ◽  
Histone H3 ◽  
Rna Expression ◽  
Genome Wide

scholarly journals RNA-directed DNA methylation prevents rapid and heritable reversal of transposon silencing under heat stress in Zea mays

PLoS Genetics ◽  
2021 ◽  
Vol 17 (6) ◽  
pp. e1009326
Author(s):  
Wei Guo ◽  
Dafang Wang ◽  
Damon Lisch
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Histone H3 ◽  
Transcriptional Silencing ◽  
Epigenetic Silencing ◽  
Terminal Inverted Repeat ◽  
Wild Type ◽  
Rna Dependent Rna Polymerase ◽  
Plant Genomes ◽  
Transposon Silencing

In large complex plant genomes, RNA-directed DNA methylation (RdDM) ensures that epigenetic silencing is maintained at the boundary between genes and flanking transposable elements. In maize, RdDM is dependent on Mediator of Paramutation 1 (Mop1), a putative RNA dependent RNA polymerase. Here we show that although RdDM is essential for the maintenance of DNA methylation of a silenced MuDR transposon in maize, a loss of that methylation does not result in a restoration of activity. Instead, heritable maintenance of silencing is maintained by histone modifications. At one terminal inverted repeat (TIR) of this element, heritable silencing is mediated via histone H3 lysine 9 dimethylation (H3K9me2), and histone H3 lysine27 dimethylation (H3K27me2), even in the absence of DNA methylation. At the second TIR, heritable silencing is mediated by histone H3 lysine 27 trimethylation (H3K27me3), a mark normally associated with somatically inherited gene silencing. We find that a brief exposure of high temperature in a mop1 mutant rapidly reverses both of these modifications in conjunction with a loss of transcriptional silencing. These reversals are heritable, even in mop1 wild-type progeny in which methylation is restored at both TIRs. These observations suggest that DNA methylation is neither necessary to maintain silencing, nor is it sufficient to initiate silencing once has been reversed. However, given that heritable reactivation only occurs in a mop1 mutant background, these observations suggest that DNA methylation is required to buffer the effects of environmental stress on transposable elements.

scholarly journals Diversification of small RNA amplification mechanisms for targeting transposon-related sequences in ciliates

2019 ◽  
Vol 116 (29) ◽  
pp. 14639-14644 ◽  
Author(s):  
Masatoshi Mutazono ◽  
Tomoko Noto ◽  
Kazufumi Mochizuki
Keyword(s):  
Transposable Elements ◽  
Small Rna ◽  
Signal Amplification ◽  
Small Rnas ◽  
Ciliated Protozoa ◽  
Rna Amplification ◽  
Somatic Nucleus ◽  
Dna Elimination ◽  
Internal Eliminated Sequences ◽  
Rna Biogenesis

The silencing of repetitive transposable elements (TEs) is ensured by signal amplification of the initial small RNA trigger, which occurs at distinct steps of TE silencing in different eukaryotes. How such a variety of secondary small RNA biogenesis mechanisms has evolved has not been thoroughly elucidated. Ciliated protozoa perform small RNA-directed programmed DNA elimination of thousands of TE-related internal eliminated sequences (IESs) in the newly developed somatic nucleus. In the ciliate Paramecium, secondary small RNAs are produced after the excision of IESs. In this study, we show that in another ciliate, Tetrahymena, secondary small RNAs accumulate at least a few hours before their derived IESs are excised. We also demonstrate that DNA excision is dispensable for their biogenesis in this ciliate. Therefore, unlike in Paramecium, small RNA amplification occurs before IES excision in Tetrahymena. This study reveals the remarkable diversity of secondary small RNA biogenesis mechanisms, even among ciliates with similar DNA elimination processes, and thus raises the possibility that the evolution of TE-targeting small RNA amplification can be traced by investigating the DNA elimination mechanisms of ciliates.

scholarly journals DNA Methylation and Histone H1 Jointly Repress Transposable Elements and Aberrant Intragenic Transcripts

2020 ◽  
Vol 77 (2) ◽  
pp. 310-323.e7 ◽  
Author(s):  
Jaemyung Choi ◽  
David B. Lyons ◽  
M. Yvonne Kim ◽  
Jonathan D. Moore ◽  
Daniel Zilberman
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Histone H1

scholarly journals DNA methylation and histone H1 cooperatively repress transposable elements and aberrant intragenic transcripts

2019 ◽  
Author(s):  
Jaemyung Choi ◽  
David B. Lyons ◽  
M. Yvonne Kim ◽  
Jonathan D. Moore ◽  
Daniel Zilberman
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Dna Methyltransferase ◽  
Housekeeping Genes ◽  
Histone H1 ◽  
List Type ◽  
Antisense Transcripts ◽  
Methylated Dna ◽  
Nucleosome Organization ◽  
Genomic Methylation

SummaryDNA methylation and histone H1 mediate transcriptional silencing of genes and transposable elements, but how they interact is unclear. In plants and animals with mosaic genomic methylation, functionally mysterious methylation is also common within constitutively active housekeeping genes. Here we show that H1 is enriched in methylated sequences, including genes, of Arabidopsis thaliana, yet this enrichment is independent of DNA methylation. Loss of H1 disperses heterochromatin, globally alters nucleosome organization, and activates H1-bound genes, but only weakly de-represses transposable elements. However, H1 loss strongly activates transposable elements hypomethylated through mutation of DNA methyltransferase MET1. Loss of H1 also activates antisense transcripts within demethylated genes. Our results demonstrate that H1 and DNA methylation cooperatively maintain transcriptional homeostasis by silencing transposable elements and aberrant intragenic transcripts. Such functionality plausibly explains why DNA methylation, a well-known mutagen, has been maintained within coding sequences of crucial plant and animal genes.HighlightsHistone H1 is enriched in methylated DNA independently of methylationLoss of H1 activates genes, alters nucleosome organization and disperses heterochromatinDNA methylation and H1 jointly silence transposonsDNA methylation and H1 cooperatively suppress intragenic antisense transcripts

scholarly journals RNA Interference in Fungi: Pathways, Functions, and Applications

2011 ◽  
Vol 10 (9) ◽  
pp. 1148-1155 ◽  
Author(s):  
Yunkun Dang ◽  
Qiuying Yang ◽  
Zhihong Xue ◽  
Yi Liu
Keyword(s):  
Gene Regulation ◽  
Rna Interference ◽  
Small Rna ◽  
Rnai Machinery ◽  
Content Type ◽  
Heterochromatin Formation ◽  
Rna Molecules ◽  
Cellular Processes ◽  
Rna Biogenesis ◽  
Core Components

ABSTRACT Small RNA molecules of about 20 to 30 nucleotides function in gene regulation and genomic defense via conserved eukaryotic RNA interference (RNAi)-related pathways. The RNAi machinery consists of three core components: Dicer, Argonaute, and RNA-dependent RNA polymerase. In fungi, the RNAi-related pathways have three major functions: genomic defense, heterochromatin formation, and gene regulation. Studies of Schizosaccharomyces pombe and Neurospora , and other fungi have uncovered surprisingly diverse small RNA biogenesis pathways, suggesting that fungi utilize RNAi-related pathways in various cellular processes to adapt to different environmental conditions. These studies also provided important insights into how RNAi functions in eukaryotic systems in general. In this review, we will discuss our current understanding of the fungal RNAi-related pathways and their functions, with a focus on filamentous fungi. We will also discuss how RNAi can be used as a tool in fungal research.

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