DNA methylation is an epigenetic modification required for transposable element (TE) silencing, genome stability, and genomic imprinting. Although DNA methylation has been intensively studied, the dynamic nature of methylation among different species has just begun to be understood. Here we summarize the recent progress in research on the wide variation of DNA methylation in different plants, organs, tissues, and cells; dynamic changes of methylation are also reported during plant growth and development as well as changes in response to environmental stresses. Overall DNA methylation is quite diverse among species, and it occurs in CG, CHG, and CHH (H = A, C, or T) contexts of genes and TEs in angiosperms. Moderately expressed genes are most likely methylated in gene bodies. Methylation levels decrease significantly just upstream of the transcription start site and around transcription termination sites; its levels in the promoter are inversely correlated with the expression of some genes in plants. Methylation can be altered by different environmental stimuli such as pathogens and abiotic stresses. It is likely that methylation existed in the common eukaryotic ancestor before fungi, plants and animals diverged during evolution. In summary, DNA methylation patterns in angiosperms are complex, dynamic, and an integral part of genome diversity after millions of years of evolution.
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CHH Methylation Islands: A Nonconserved Feature of Grass Genomes That Is Positively Associated with Transposable Elements but Negatively Associated with Gene-Body Methylation
Abstract Methylated CHH (mCHH) islands are peaks of CHH methylation that occur primarily upstream to genes. These regions are actively targeted by the methylation machinery, occur at boundaries between heterochromatin and euchromatin, and tend to be near highly expressed genes. Here we took an evolutionary perspective by studying upstream mCHH islands across a sample of eight grass species. Using a statistical approach to define mCHH islands as regions that differ from genome-wide background CHH methylation levels, we demonstrated that mCHH islands are common and associate with 39% of genes, on average. We hypothesized that islands should be more frequent in genomes of large size, because they have more heterochromatin and hence more need for defined boundaries. We found, however, that smaller genomes tended to have a higher proportion of genes associated with 5′ mCHH islands. Consistent with previous work suggesting that islands reflect the silencing of the edge of transposable elements (TEs), genes with nearby TEs were more likely to have mCHH islands. However, the presence of mCHH islands was not a function solely of TEs, both because the underlying sequences of islands were often not homologous to TEs and because genic properties also predicted the presence of 5′ mCHH islands. These genic properties included length and gene-body methylation (gbM); in fact, in three of eight species, the absence of gbM was a stronger predictor of a 5′ mCHH island than TE proximity. In contrast, gene expression level was a positive but weak predictor of the presence of an island. Finally, we assessed whether mCHH islands were evolutionarily conserved by focusing on a set of 2,720 orthologs across the eight species. They were generally not conserved across evolutionary time. Overall, our data establish additional genic properties that are associated with mCHH islands and suggest that they are not just a consequence of the TE silencing machinery.
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- Award ID(s):
- 1655808
- NSF-PAR ID:
- 10354718
- Editor(s):
- Lerat, Emmanuelle
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 13
- Issue:
- 8
- ISSN:
- 1759-6653
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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In plants and mammals, DNA methylation plays a critical role in transcriptional silencing by delineating heterochromatin from transcriptionally active euchromatin. A homeostatic balance between heterochromatin and euchromatin is essential to genomic stability. This is evident in many diseases and mutants for heterochromatin maintenance, which are characterized by global losses of DNA methylation coupled with localized ectopic gains of DNA methylation that alter transcription. Furthermore, we have shown that genome-wide methylation patterns in
Arabidopsis thaliana are highly stable over generations, with the exception of rare epialleles. However, the extent to which natural variation in the robustness of targeting DNA methylation to heterochromatin exists, and the phenotypic consequences of such variation, remain to be fully explored. Here we describe the finding that heterochromatin and genic DNA methylation are highly variable among 725A. thaliana accessions. We found that genic DNA methylation is inversely correlated with that in heterochromatin, suggesting that certain methylation pathway(s) may be redirected to genes upon the loss of heterochromatin. This redistribution likely involves a feedback loop involving the DNA methyltransferase, CHROMOMETHYLASE 3 (CMT3), H3K9me2, and histone turnover, as highly expressed, long genes with a high density of CMT3-preferred CWG sites are more likely to be methylated. Importantly, although the presence of CG methylation in genes alone may not affect transcription, genes containing CG methylation are more likely to become methylated at non-CG sites and silenced. These findings are consistent with the hypothesis that natural variation in DNA methylation homeostasis may underlie the evolution of epialleles that alter phenotypes. -
Transposable elements (TEs) are sequences that replicate and move throughout genomes, and they can be silenced through methylation of cytosines at CpG dinucleotides. TE abundance contributes to genome size, but TE silencing variation across genomes of different sizes remains underexplored. Salamanders include most of the largest C-values – 9 to 120 Gb. We measured CpG methylation levels in salamanders with genomes ranging from 2N = ∼58 Gb to 4N = ∼116 Gb. We compared these levels to results from endo- and ectothermic vertebrates with more typical genomes. Salamander methylation levels are approximately 90%, higher than all endotherms. However, salamander methylation does not differ from other ectotherms, despite an approximately 100-fold difference in nuclear DNA content. Because methylation affects the nucleotide compositional landscape through 5-methylcytosine deamination to thymine, we quantified salamander CpG dinucleotide levels and compared them to other vertebrates. Salamanders and other ectotherms have comparable CpG levels, and ectotherm levels are higher than endotherms. These data show no shift in global methylation at the base of salamanders, despite a dramatic increase in TE load and genome size. This result is reconcilable with previous studies that considered endothermy and ectothermy, which may be more important drivers of methylation in vertebrates than genome size.more » « less
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Plant genomes are littered with transposable elements (TEs). Because TEs are potentially highly mutagenic, host organisms have evolved a set of defense mechanisms to recognize and epigenetically silence them. Although the maintenance of TE silencing is well studied, our understanding of the initiation of TE silencing is limited, but it clearly involves small RNAs and DNA methylation. Once TEs are silent, the silent state can be maintained to subsequent generations. However, under some circumstances, such inheritance is unstable, leading to the escape of TEs to the silencing machinery, resulting in the transcriptional activation of TEs. Epigenetic control of TEs has been found to be closely linked to many other epigenetic phenomena, such as genomic imprinting, and is known to contribute to regulation of genes, especially those near TEs. Here we review and discuss the current models of TE silencing, its unstable inheritance after hybridization, and the effects of epigenetic regulation of TEs on genomic imprinting.more » « less
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SUMMARY The DOMAINS REARRANGED METHYLTRANSFERASEs (DRMs) are crucial for RNA‐directed DNA methylation (RdDM) in plant species.
Setaria viridis is a model monocot species with a relatively compact genome that has limited transposable element (TE) content. CRISPR‐based genome editing approaches were used to create loss‐of‐function alleles for the two putative functional DRM genes inS .viridis to probe the role of RdDM. Double mutant (drm1ab) plants exhibit some morphological abnormalities but are fully viable. Whole‐genome methylation profiling provided evidence for the widespread loss of methylation in CHH sequence contexts, particularly in regions with high CHH methylation in wild‐type plants. Evidence was also found for the locus‐specific loss of CG and CHG methylation, even in some regions that lack CHH methylation. Transcriptome profiling identified genes with altered expression in thedrm1ab mutants. However, the majority of genes with high levels of CHH methylation directly surrounding the transcription start site or in nearby promoter regions in wild‐type plants do not have altered expression in thedrm1ab mutant, even when this methylation is lost, suggesting limited regulation of gene expression by RdDM. Detailed analysis of the expression of TEs identified several transposons that are transcriptionally activated indrm1ab mutants. These transposons are likely to require active RdDM for the maintenance of transcriptional repression.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/gbe/evab144
