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Dnmt1-Independent CG Methylation Contributes to Nucleosome Positioning in Diverse Eukaryotes

ABSTRACT: Dnmt1 epigenetically propagates symmetrical CG methylation in many eukaryotes. Their genomes are typically depleted of CG dinucleotides because of imperfect repair of deaminated methylcytosines. Here, we extensively survey diverse species lacking Dnmt1 and show that, surprisingly, symmetrical CG methylation is nonetheless frequently present and catalyzed by a different DNA methyltransferase family, Dnmt5. Numerous Dnmt5-containing organisms that diverged more than a billion years ago exhibit clustered methylation, specifically in nucleosome linkers. Clustered methylation occurs at unprecedented densities and directly disfavors nucleosomes, contributing to nucleosome positioning between clusters. Dense methylation is enabled by a regime of genomic sequence evolution that enriches CG dinucleotides and drives the highest CG frequencies known. Species with linker methylation have small, transcriptionally active nuclei that approach the physical limits of chromatin compaction. These features constitute a previously unappreciated genome architecture, in which dense methylation influences nucleosome positions, likely facilitating nuclear processes under extreme spatial constraints.

ORGANISM(S): Fragilariopsis cylindrus Leishmania major Emiliania huxleyi Micromonas pusilla Thalassiosira pseudonana Ostreococcus sp. 'lucimarinus' Bathycoccus prasinos Aureococcus anophagefferens Cryptococcus neoformans var. grubii Cyanidioschyzon merolae Phaeodactylum tricornutum

PROVIDER: GSE46692 | GEO | 2014/03/13

SECONDARY ACCESSION(S): PRJNA201680

REPOSITORIES: GEO

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Dnmt1-Independent CG Methylation Contributes to Nucleosome Positioning in Diverse Eukaryotes

Project description:Dnmt1 epigenetically propagates symmetrical CG methylation in many eukaryotes. Their genomes are typically depleted of CG dinucleotides because of imperfect repair of deaminated methylcytosines. Here, we extensively survey diverse species lacking Dnmt1 and show that, surprisingly, symmetrical CG methylation is nonetheless frequently present and catalyzed by a different DNA methyltransferase family, Dnmt5. Numerous Dnmt5-containing organisms that diverged more than a billion years ago exhibit clustered methylation, specifically in nucleosome linkers. Clustered methylation occurs at unprecedented densities and directly disfavors nucleosomes, contributing to nucleosome positioning between clusters. Dense methylation is enabled by a regime of genomic sequence evolution that enriches CG dinucleotides and drives the highest CG frequencies known. Species with linker methylation have small, transcriptionally active nuclei that approach the physical limits of chromatin compaction. These features constitute a previously unappreciated genome architecture, in which dense methylation influences nucleosome positions, likely facilitating nuclear processes under extreme spatial constraints. DNA methylation, RNA and nucleosome sequencing data for diverse eukaryotes

2014-03-13 | E-GEOD-46692 | biostudies-arrayexpress

Evolutionary persistence of DNA methylation for millions of years after ancient loss of a de novo methyltransferase

Project description:Cytosine methylation of DNA is a widespread modification of DNA that plays numerous critical roles, yet has been lost many times in diverse eukaryotic lineages. In the yeast Cryptococcus neoformans, CG methylation occurs in transposon-rich repeats and requires the DNA methyltransferase, Dnmt5. We show that Dnmt5 displays exquisite maintenance-type specificity in vitro and in vivo and utilizes similar in vivo cofactors as the metazoan maintenance methylase Dnmt1. Remarkably, phylogenetic and functional analysis revealed that the ancestral species lost the gene for a de novo methylase, DnmtX, between 50-150 MYA. We examined how methylation has persisted since the ancient loss of DnmtX. Experimental and comparative studies reveal efficient replication of methylation patterns in C. neoformans, rare stochastic methylation loss and gain events, and the action of natural selection. We propose that an epigenome has been propagated for >50 MY through a process analogous to Darwinian evolution of the genome.

2020-01-19 | GSE134684 | GEO

Non-CG methylation is more potent than CG methylation in moss genome regulation [Athaliana RNA-Seq]

Project description:Cytosine methylation is commonly targeted to symmetrical CG sites, as well as to non-CGs, such as the symmetrical-CHG and asymmetric-CHH sites in plants (H= A, C or T). Thus far, depletion of CG methylation in plants was associated with ample transcriptional activation of transposons. Here, we profiled transcription in various context specific methylation mutants in the early-diverged plant, Physcomitrella patens. We discovered that specific elimination of CG methylation is fully complemented by non-CG methylation but not vice versa. Between the symmetrically-methylated sites, CHG methylation silenced transposons stronger than CG methylation did. Finally, non-CG methylation revealed as crucial for the silencing of CG depleted transposons. Our results suggest that non-CG methylation evolved to silence transposons due to functional limitations and/or rapid mutability of methylated-CGs.

2020-12-30 | GSE142052 | GEO

Non-CG methylation is more potent than CG methylation in moss genome regulation [Ppatens RNA-Seq]

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Non-CG methylation is more potent than CG methylation in moss genome regulation [Ppatens BS-Seq]

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Dnmt1-Independent CG Methylation Contributes to Nucleosome Positioning in Diverse Eukaryotes

Project description:Dnmt1-Independent CG Methylation Contributes to Nucleosome Positioning in Diverse Eukaryotes

| PRJNA201680 | ENA

DDM1/Lsh remodelers allow methylation of DNA wrapped in nucleosomes

Project description:Eukaryotic DNA is wrapped around histone octamers to form nucleosomes, which are separated by linker DNA bound by histone H1. In many species, the DNA exhibits methylation of CG dinucleotides, which is epigenetically inherited via a semiconservative mechanism. How methyltransferases access DNA within nucleosomes remains mysterious. Here we show that methylation of nucleosomes requires DDM1/Lsh nucleosome remodelers in Arabidopsis thaliana and mouse. We also show that removal of histone H1, which partially restores methylation in ddm1 mutants, does so primarily in the linker DNA between nucleosomes. In h1ddm1 compound mutants, substantial portions of the genome exhibit dramatically periodic methylation that approaches wild-type levels in linker DNA but is virtually absent in nucleosomes. We also present evidence that de novo methylation supplements semiconservative maintenance of CG methylation across generations. Overall, our results demonstrate that nucleosomes and H1 are barriers to DNA methylation, which are overcome by DDM1/Lsh nucleosome remodelers.

2017-11-15 | GSE96994 | GEO

CG dinucleotides enhance promoter activity independent of DNA methylation

Project description:CG dinucleotides enhance promoter activity independent of DNA methylation

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A balance of de novo and maintenance activities governs epigenetic inheritance of CG methylation in Arabidopsis transposons

Project description:Dnmt1/MET1 methyltransferases mediate the epigenetic inheritance of cytosine methylation within CG dinucleotides (mCG). These enzymes use a semiconservative mechanism previously expected to produce binary present/absent methylation patterns. However, we show here that in Arabidopsis thaliana h1ddm1 mutants, intermediate heterochromatic mCG is quantitatively associated with transposon expression and is stably inherited across many generations. We develop a mathematical model that estimates the rates of semiconservative maintenance failure and de novo methylation at each transposon, demonstrating that mCG can be stably inherited at any level via a dynamical balance of these activities. We find that DRM2 – the core methyltransferase of the RNA-directed DNA methylation pathway – catalyzes most of the heterochromatic de novo mCG, with de novo rates orders of magnitude higher than previously thought, whereas chromomethylases make smaller contributions. Our results demonstrate that mCG epigenetic inheritance in plant heterochromatin is highly dynamic, with CG sites frequently switching methylation states.

2023-02-17 | GSE197718 | GEO

A quantitative model of MET1-catalyzed establishment and epigenetic inheritance of DNA methylation

Project description:Methylation of CG dinucleotides (mCG), which regulates genome function in eukaryotes, is epigenetically propagated by Dnmt1/MET1 methyltransferases via a semiconservative mechanism. How these enzymes accomplish stable epigenetic inheritance despite imperfect fidelity remains mysterious. Here we show that MET1 de novo activity, which is enhanced by existing proximate methylation, seeds and stabilizes mCG in Arabidopsis thaliana genes. MET1 activity is delimited by active DNA demethylation and counterbalanced by histone variant H2A.Z, natural variation in which accounts for high genic methylation in accessions from northern Sweden. Based on these observations, we develop a mathematical model that precisely recapitulates mCG inheritance dynamics and successfully predicts steady-state intragenic mCG patterns and their population-scale variation given only CG site spacing as input. Our results demonstrate how methylation patterns are created in plant genes, reconcile imperfect mCG maintenance with long-term stability, and establish a quantitative model for the epigenetic inheritance of mCG.

2023-11-13 | GSE204837 | GEO

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