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Mechanistic insights into plant SUVH family H3K9 methyltransferases and their binding to context-biased non-CG DNA methylation

ABSTRACT: DNA methylation functions in gene silencing and the maintenance of genome integrity. In plants, non-CG DNA methylation is linked through a self-reinforcing loop with histone 3 lysine 9 dimethylation (H3K9me2). The plant-specific SUPPRESSOR OF VARIEGATION 3–9 HOMOLOG (SUVH) family H3K9 methyltransferases (MTases) bind to DNA methylation marks and catalyze H3K9 methylation. Here, we analyzed the structure and function of Arabidopsis thaliana SUVH6 to understand how this class of enzyme maintains methylation patterns in the genome. We reveal that SUVH6 has a distinct 5mC base-flipping mechanism involving a thumb loop element. Autoinhibition of H3 substrate entry is regulated by a SET domain loop, and a conformational transition in the postSET domain upon cofactor binding may control catalysis. In vitro DNA binding and in vivo ChIP-seq data reveal that the different SUVH family H3K9 MTases have distinct DNA binding preferences, targeting H3K9 methylation to sites with different methylated DNA sequences, explaining the context biased non-CG DNA methylation in plants.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE114009 | GEO | 2018/08/17

REPOSITORIES: GEO

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Mechanistic insights into plant SUVH family H3K9 methyltransferases and their binding to context-biased non-CG DNA methylation

Project description:Mechanistic insights into plant SUVH family H3K9 methyltransferases and their binding to context-biased non-CG DNA methylation

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Project description:To investigate the impact of disruption of the non-CG DNA methylation/H3K9me2 pathway upon transcription in Arabidopsis, we performed RNA-seq using meiotic-stage floral buds from wild type (Col-0) and kyp/suvh4 suvh5 suvh6 mutant plants. This enabled identification of differentially expressed genes and transposable elements (TEs). TEs that were up-regulated in kyp/suvh4 suvh5 suvh6 relative to wild type were evaluated for over-representation of elements within each TE family.

2020-01-21 | E-MTAB-7371 | biostudies-arrayexpress

Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis

Project description:DNA methylation occurs in both CG and non-CG sequence contexts. Non-CG methylation is abundant in plants, and is mediated by CHROMOMETHYLASE (CMT) and DOMAINS REARRANGED METHYLTRANSFERASE (DRM) proteins; however its roles remain poorly understood. Here we characterize the roles of non-CG methylation in Arabidopsis thaliana. We show that a poorly characterized methyltransferase, CMT2, is a functional methyltransferase in vitro and in vivo. CMT2 specifically binds histone H3 lysine 9 (H3K9) dimethylation and methylates non-CG cytosines at sites that are also regulated by H3K9 dimethylation. By generating different combinations of non-CG methylation mutants, we reveal the contributions and redundancies between each methyltransferase in DNA methylation patterning and in regulating transposable elements (TEs) and protein-coding genes. We also demonstrate extensive dependencies of small RNA accumulation and H3K9 methylation patterning on non-CG methylation, suggesting self-reinforcing mechanisms between these epigenetic factors. The results suggest that non-CG methylation patterns are critical in shaping the histone modification and small non-coding RNA landscapes.

2013-12-15 | GSE51304 | GEO

Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis

2013-12-15 | E-GEOD-51304 | biostudies-arrayexpress

Genome-wide analysis of H3K9me2 in ibm1, kyp, and cmt3 mutants of Arabidopsis thaliana

2010-09-21 | GSE22953 | GEO

Meiotic cohesin, chromatin and expression profiling of Arabidopsis thaliana floral buds from wild type and non-CG DNA methylation/H3K9me2 pathway mutant plants (ChIP-seq)

Project description:We generated and sequenced ChIP libraries for the meiotic cohesin subunit REC8 and four histone modifications (H3K4me1, H3K4me2, H3K9me2 and H3K27me1) to investigate their relationships with meiotic chromosome architecture and recombination in Arabidopsis thaliana. REC8 and H3K9me2 ChIP-seq were performed using meiotic-stage floral buds from wild type (Col-0) and non-CG DNA methylation/H3K9me2 pathway mutant (kyp/suvh4 suvh5 suvh6 or cmt3) plants to examine the role of heterochromatin assembly in meiotic cohesin distribution.

2020-01-21 | E-MTAB-7370 | biostudies-arrayexpress

The Epigenomic Landscape of Prokaryotes

Project description:DNA methylation is an important regulator of genome function in the eukaryotes, but it is currently unclear if the same is true in prokaryotes. While regulatory functions have been demonstrated for a small number of bacteria, there have been no large-scale studies of prokaryotic methylomes and the full repertoire of targets and biological functions of DNA methylation remains unclear. Here we applied single-molecule, real-time sequencing to directly study the methylomes of 232 phylogenetically diverse prokaryotes. Collectively, we identified 834 methylated motifs, enabling the specific annotation of 415 DNA methyltransferases (MTases), and adding substantially to existing databases of MTase specificities. While the majority of MTases function as components of restriction-modification systems, 139 MTases have no cognate restriction enzyme in the genome, suggesting some other functional role. Several of these âorphanâ MTases are conserved across species and exhibit patterns of DNA methylation consistent with known regulatory MTases. Based on these patterns of methylation, we identify candidate novel regulators of gene expression in several phyla of bacteria, and candidate regulators of DNA replication in Haloarchaea. Together these data substantially advance our knowledge of DNA restriction-modification systems, and hint at a wider role for methylation in prokaryotic genome regulation. Single-molecule, real-time sequencing of DNA modifications across 232 diverse prokaryotic genomes.

2016-01-20 | E-GEOD-69872 | biostudies-arrayexpress

Genome-wide analysis of H3K9me2 in ibm1, kyp, and cmt3 mutants of Arabidopsis thaliana

Project description:In diverse eukaryotes, constitutively silent sequences, such as transposons and repeats, are marked by methylation at histone H3 lysine 9 (H3K9me). Despites the conservation and importance in the genome integrity, mechanisms to exclude H3K9m from active genes remained largely unexplored. Here we show in Arabidopsis that the exclusion depends on a histone demethylase gene, IBM1 (increase in BONSAI methylation); loss-of-function ibm1 mutation caused ectopic H3K9me in thousands of genes, which accompanies genic DNA methylation at non-CG sites. The ibm1-induced genic H3K9me depended on both histone methylase KYP/SUVH4 and DNA methylase CMT3, suggesting interdependence of two epigenetic marks – H3K9me and non-CG methylation. Notably, IBM1 enhanced loss of H3K9m in transcriptionally de-repressed sequences. Furthermore, disruption of transcription in genes induced ectopic non-CG methylation, mimicking the loss of IBM1 function. We propose that active chromatin is stabilized by the autocatalytic loop of transcription and H3K9 demethylation. This process counteracts accumulation of silent epigenetic marks, H3K9me and non-CG methylation, which is also autocatalytic. Leaves of 4-week-old plants were fixed as described previously (Saze et al, 2008). Chromatin immunoprecipitation (ChIP) was performed as described previously (Kimura et al, 2008), using antibody against H3K9me2 (CMA307, Kimura et al, 2008, PMID: 18227620). Non-immunoprecipitated DNA (input DNA) and ChIP samples were amplified, labeled, and hybridized to microarray according to the manufacturer’s instruction (Protocols for Chromatin Immunoprecipitation and Amplification, NimbleGen). Input DNA and ChIP DNA were differentially labeled with Cy3 and Cy5, respectively, and competitively hybridized to a microarray chip. We used NimbleGen 2.1M HD2 array covering entire genome of A. thaliana.

2010-09-21 | E-GEOD-22953 | biostudies-arrayexpress

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Project description:DNA methylation is an important regulator of genome function in the eukaryotes, but it is currently unclear if the same is true in prokaryotes. While regulatory functions have been demonstrated for a small number of bacteria, there have been no large-scale studies of prokaryotic methylomes and the full repertoire of targets and biological functions of DNA methylation remains unclear. Here we applied single-molecule, real-time sequencing to directly study the methylomes of 232 phylogenetically diverse prokaryotes. Collectively, we identified 834 methylated motifs, enabling the specific annotation of 415 DNA methyltransferases (MTases), and adding substantially to existing databases of MTase specificities. While the majority of MTases function as components of restriction-modification systems, 139 MTases have no cognate restriction enzyme in the genome, suggesting some other functional role. Several of these ‘orphan’ MTases are conserved across species and exhibit patterns of DNA methylation consistent with known regulatory MTases. Based on these patterns of methylation, we identify candidate novel regulators of gene expression in several phyla of bacteria, and candidate regulators of DNA replication in Haloarchaea. Together these data substantially advance our knowledge of DNA restriction-modification systems, and hint at a wider role for methylation in prokaryotic genome regulation.

2016-01-20 | GSE69872 | GEO

MYCOPLASMAL DNA METHYLTRANSFERASES ALTER THE EPIGENETIC LANDSCAPE IN HUMAN CELLS

Project description:Aberrant DNA methylation is frequently observed in human disease, particularly in cancer, but the underlying pathogenic mechanisms are not well understood. We demonstrate that mycoplasmal 5-methylcytosine DNA methyltransferases (MTases) can induce epigenetic alterations in human cells. We expressed the CG-specific Mhy1 and the GATC-specific Mhy2 Mycoplasma hyorhinis MTases in cultured human cells, and determined that both enzymes penetrated the cell nuclei and induced a 3.5-fold and a 2-fold increase in genome-wide methylation, respectively. We next mapped genomic locations of these de novo methylation marks in the human genome. Sequence analysis suggested that most gene loci became hypermethylated, except the promoters of actively transcribed genes, which appeared to be protected from methylation by these exogenous MTs. Significant aberrant de novo methylation of cytosines within the GATC sequences were induced by Mhy2 in non-cancer HTR8/SVneo trophoblasts. This included a striking activation of cell proliferation pathways via upregulation of c-JUN and MYC oncogenes and transcription factors, including ATF3, KLF6 and DKK1. Our findings unveil a novel link between the microbiome and human epigenetics with special relevance to cancer epigenetics.

2015-03-01 | GSE53853 | GEO

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