Epimutations are associated with CHROMOMETHYLASE 3-induced de novo DNA methylation

Wendte, Jered M.; Zhang, Yinwen; Ji, Lexiang; Shi, Xiulin; Hazarika, Rashmi R.; Shahryary, Yadollah; Johannes, Frank; Schmitz, Robert J.

doi:10.7554/elife.47891

Cited by 68 publications

(115 citation statements)

References 78 publications

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“…The observed levels were still an order of magnitude higher than the pure background noise that can be inferred from chloroplast methylation, especially in the case of CHG (1.16% CHG methylation on average over gene body compared to 0.22% background) ( Fig. S2, Table S1c), consistent with the known presence of low levels of non-CG methylation in gene bodies [31]. In terms of methylation in TEs, EM-seq produces similar metaplot pro les as WGBS, albeit with lower levels (especially for CHG and CHH ( Fig.…”

Section: Arabidopsis Dna Methylation Levels Measured By Em-seq and Wgbssupporting

confidence: 73%

Efficient and Accurate Determination of Genome-Wide DNA Methylation Patterns in Arabidopsis with Enzymatic Methyl Sequencing.

Feng

Zhong

Wang

et al. 2020

Preprint

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Background: 5’ methylation of cytosines in DNA molecules is an important epigenetic mark in eukaryotes. Bisulfite sequencing is the gold standard of DNA methylation detection, and whole-genome bisulfite sequencing (WGBS) has been widely used to detect methylation at single-nucleotide resolution on a genome-wide scale. However, sodium bisulfite is known to severely degrade DNA, which, in combination with biases introduced during PCR amplification, leads to unbalanced base representation in the final sequencing libraries. Enzymatic conversion of unmethylated cytosines to uracils can achieve the same end product for sequencing as does bisulfite treatment and does not affect the integrity of the DNA; enzymatic methylation sequencing may thus provide advantages over bisulfite sequencing.Results: Using an enzymatic methyl-seq (EM-seq) technique to selectively deaminate unmethylated cytosines to uracils, we generated and sequenced libraries based on different amounts of Arabidopsis input DNA and different numbers of PCR cycles, and compared these data to results from traditional whole genome bisulfite sequencing. We found that EM-seq libraries were more consistent between replicates and had higher mapping and lower duplication rates, lower background noise, higher average coverage, and higher coverage of total cytosines. Differential methylation region (DMR) analysis showed that WGBS tended to over-estimate methylation levels especially in CHG and CHH contexts, whereas EM-seq detected higher CG methylation levels in certain highly methylated areas. These phenomena can be mostly explained by a correlation of WGBS methylation estimation with GC content and methylated cytosine density. We used EM-seq to compare methylation between leaves and flowers, and found that CHG methylation level is greatly elevated in flowers, especially in pericentromeric regions. Conclusion: We suggest that EM-seq is a more accurate and reliable approach than WGBS to detect methylation. Compared to WGBS, the results of EM-seq are less affected by differences in library preparation conditions or by the skewed base composition in the converted DNA. It may therefore be more desirable to use EM-seq in methylation studies.

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Section: Arabidopsis Dna Methylation Levels Measured By Em-seq and Wgbssupporting

confidence: 73%

Efficient and Accurate Determination of Genome-Wide DNA Methylation Patterns in Arabidopsis with Enzymatic Methyl Sequencing.

Feng

Zhong

Wang

et al. 2020

Preprint

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“…We speculate that additional data on DNA methylation in P. patens may reveal shared features of gene body methylation with M. polymorpha and with flowering plants. More shared features across land plants would provide additional support for the currently proposed model that gene body methylation may be a natural consequence of CMT3 function in the maintenance of heterochromatin (Wendte et al , ). Although bryophytes do not have CMT3‐clade CMT genes (Noy et al , ), de novo CG and CHH methylation activity of DNMT3 homologues in heterochromatic regions may provide a potential mechanism for how gene body methylation may arise in bryophytes (Yaari et al , ).…”

Section: Discussionmentioning

confidence: 75%

“…The functional and evolutionary significance of gene body methylation in the lineages of land plants is highly debated (Takuno et al , ; Zilberman, ; Bewick and Schmitz, ; Bewick et al , ; Wendte et al , ). Some studies have reported that gene body methylated genes are present in bryophytes, whereas others argued that they are just artefactual in origin (Zemach et al , ; Fulneckova et al , ; Takuno et al , ).…”

Section: Discussionmentioning

confidence: 99%

A pseudomolecule‐scale genome assembly of the liverwort Marchantia polymorpha

et al. 2019

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Summary Marchantia polymorpha has recently become a prime model for cellular, evo‐devo, synthetic biological, and evolutionary investigations. We present a pseudomolecule‐scale assembly of the M. polymorpha genome, making comparative genome structure analysis and classical genetic mapping approaches feasible. We anchored 88% of the M. polymorpha draft genome to a high‐density linkage map resulting in eight pseudomolecules. We found that the overall genome structure of M. polymorpha is in some respects different from that of the model moss Physcomitrella patens. Specifically, genome collinearity between the two bryophyte genomes and vascular plants is limited, suggesting extensive rearrangements since divergence. Furthermore, recombination rates are greatest in the middle of the chromosome arms in M. polymorpha like in most vascular plant genomes, which is in contrast with P. patens where recombination rates are evenly distributed along the chromosomes. Nevertheless, some other properties of the genome are shared with P. patens. As in P. patens, DNA methylation in M. polymorpha is spread evenly along the chromosomes, which is in stark contrast with the angiosperm model Arabidopsis thaliana, where DNA methylation is strongly enriched at the centromeres. Nevertheless, DNA methylation and recombination rate are anticorrelated in all three species. Finally, M. polymorpha and P. patens centromeres are of similar structure and marked by high abundance of retroelements unlike in vascular plants. Taken together, the highly contiguous genome assembly we present opens unexplored avenues for M. polymorpha research by linking the physical and genetic maps, making novel genomic and genetic analyses, including map‐based cloning, feasible.

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“…CHH methylation can be classified as CWA (W = A or T) or non-CWA. DRM2 methylates CWA and non-CWA sites, and CMT2 preferentially methylates CWA nucleotides [53][54][55] . Only the edges of long heterochromatic TEs were hypomethylated in non-CWA contexts of post-embryonic nrpd1a mutant tissues relative to wild type ( Fig.…”

Section: Small Rna-directed Methylation Of Transposons During Embryogmentioning

confidence: 99%

Chromatin Regulates Bipartite-Classified Small RNA Expression to Maintain Epigenome Homeostasis in Arabidopsis

Papareddy

Páldi

Paulraj

et al. 2020

Preprint

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Eukaryotic genomes are partitioned into euchromatic and heterochromatic domains to regulate gene expression and other fundamental cellular processes. However, chromatin is dynamic during growth and development, and must be properly re-established after its decondensation. Small interfering RNAs (siRNAs) promote heterochromatin formation in eukaryotes, but little is known about how chromatin regulates siRNA transcription. We demonstrated that thousands of transposable elements (TEs) produce exceptionally high levels of siRNAs in Arabidopsis thaliana embryos. Depending on whether they are located in euchromatic or heterochromatic regions of the genome, bipartite-classified TEs generate siRNAs throughout embryogenesis according to two distinct patterns. siRNAs are transcribed in embryos and required to direct the re-establishment of DNA methylation on TEs from which they are derived in the new generation. Decondensed chromatin also permits the production of 24-nt siRNAs from heterochromatic TEs during post-embryogenesis, and siRNA production from bipartite-classified TEs is controlled by their chromatin states. Decondensation of heterochromatin in response to developmental, and perhaps environmental, cues promotes the transcription and function of siRNAs in plants. Our results indicate that chromatin-mediated siRNA transcription provides a cell-autonomous homeostatic control mechanism to reconstitute pre-existing chromatin states during growth and development including those that ensure silencing of TEs in the future germ line.

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Epimutations are associated with CHROMOMETHYLASE 3-induced de novo DNA methylation

Cited by 68 publications

References 78 publications

Efficient and Accurate Determination of Genome-Wide DNA Methylation Patterns in Arabidopsis with Enzymatic Methyl Sequencing.

Efficient and Accurate Determination of Genome-Wide DNA Methylation Patterns in Arabidopsis with Enzymatic Methyl Sequencing.

A pseudomolecule‐scale genome assembly of the liverwort Marchantia polymorpha

Chromatin Regulates Bipartite-Classified Small RNA Expression to Maintain Epigenome Homeostasis in Arabidopsis

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