Phylogenetic shifts in gene body methylation correlate with gene expression and reflect trait conservation

Seymour, Danelle K.; Gaut, Brandon S.

doi:10.1101/687186

Cited by 7 publications

(13 citation statements)

References 65 publications

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“…Conservation and phenomenological coherence suggest important functions 21 . Indeed, gbM is associated with (small) gene expression differences across plant species 26,27 , represses aberrant intragenic transcripts 28 , and appears to be under natural selection 26,29,30 . Moreover, loss of methyltransferase function causes developmental abnormalities in honeybees 31 , animals in which methylation is principally restricted to gene bodies 32 .…”

mentioning

confidence: 99%

Epigenetic inheritance mediates phenotypic diversity in natural populations

Shahzad

Moore

Zilberman

2021

Preprint

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Cytosine methylation is an epigenetically heritable DNA modification common in plant and animal genes, but the functional and evolutionary significance of gene body methylation (gbM) has remained enigmatic. Here we show that gbM enhances gene expression in Arabidopsis thaliana. We also demonstrate that natural gbM variation influences drought and heat tolerance and flowering time by modulating gene expression, including that of Flowering Locus C (FLC). Notably, epigenetic variation accounts for as much trait heritability in natural populations as DNA sequence polymorphism. Furthermore, we identify gbM variation in numerous genes associated with environmental variables, including a strong association between flowering time, spring atmospheric NO2 - a by-product of fossil fuel burning - and FLC epialleles. Our study demonstrates that gbM is an important modulator of gene expression, and its natural variation fundamentally shapes phenotypic diversity in plant populations. Thus, gbM provides an epigenetic basis for adaptive evolution independent of genetic polymorphism.

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confidence: 99%

Epigenetic inheritance mediates phenotypic diversity in natural populations

Shahzad

Moore

Zilberman

2021

Preprint

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“…However, whether gene body methylation directly regulates levels of gene expression has been controversial 52,53 . Phylogenetic analyses of methylated and unmethylated plant species as well as analyses of within-species variation of gene body methylation in plants 52,53,54 Our results point to the middle blastoderm stage as the crucial point where Nv-Dnmt1a has its strongest effects on the embryonic transcriptome. Our data also show that the indirect effects of Nv-Dnmt1a pRNAi are mediated by both disruption of mRNA degradation, and misregulation of transcription from the zygotic genome.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies posited that gene body methylation has an important role in facilitating high, steady levels of gene expression 17,36 . However, whether gene body methylation directly regulates levels of gene expression has been controversial 54,55 . Phylogenetic analyses of methylated and unmethylated plant species as well as analyses of within-species variation of gene body methylation in plants 54,55,56 led to at most weak effects of gene body methylation on gene expression, although the evolutionary conservation of gene body methylation indicated associated functionality.…”

Section: Discussionmentioning

confidence: 99%

“…However, whether gene body methylation directly regulates levels of gene expression has been controversial 54,55 . Phylogenetic analyses of methylated and unmethylated plant species as well as analyses of within-species variation of gene body methylation in plants 54,55,56 led to at most weak effects of gene body methylation on gene expression, although the evolutionary conservation of gene body methylation indicated associated functionality. Here we show that as a result of pRNAi of Nv-Dnmt1a, the vast majority of methylated genes that are differentially expressed show reduction of gene expression.…”

Section: Discussionmentioning

confidence: 99%

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Dnmt1a is essential for gene body methylation and the regulation of zygotic genome activation in the wasp

Arsala

et al. 2021

Preprint

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Gene body methylation (GBM) is an ancestral form of DNA methylation whose role in development has remained unclear. Unlike vertebrates, DNA methylation is found exclusively in gene bodies in the wasp Nasonia vitripennis, which provides a unique opportunity to interpret the role of GBM in development. We confirmed that parental RNAi (pRNAi) knockdown of DNMT1 (Nv-Dnmt1a) in Nasonia leads to embryonic lethality and failures in cellularization and morphogenesis. Using whole-genome bisulfite sequencing, we found a widespread loss of GBM in Nv-Dnmt1a pRNAi embryos. Using RNAseq, we found that methylated genes that lost GBM in the pRNAi samples were exclusively downregulated during zygotic genome activation. Unexpectedly, nearly all affected unmethylated genes were up-regulated after pRNAi. Lack of proper clearance of mRNAs and abnormal activation drive this up-regulation, indicating critical roles for Nv-Dnmt1a and GBM in the maternal-zygotic transition (MZT) in the wasp, despite their absence in Drosophila.

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“…For example, Takuno et al (2016) 37 showed that only 6% of genes in rice have high levels (>90%) of CG methylation compared to 24% of genes in the much larger (2,300 Mb) genome of maize. The contrast is even stronger for high (>90%) CHG methylation -12% vs. 1% of maize and rice genes, respectively -reflecting the strong positive correlation between gene CHG methylation and genome size [37][38][39] .…”

Section: Introductionmentioning

confidence: 98%

Gene capture by transposable elements leads to epigenetic conflict in maize

Muyle¹,

Seymour²,

Darzentas

et al. 2019

Preprint

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Plant transposable elements (TEs) regularly capture fragments of host genes. When the host employs siRNAs to silence these TEs, siRNAs homologous to the captured regions may target both the TEs and the genes, potentially leading to their silencing. This epigenetic cross-talk establishes an intragenomic conflict: silencing the TEs comes with the potential cost of silencing the genes. If the genes are important, however, natural selection will act to maintain function by moderating the silencing response. Such moderation may advantage the TEs. Here, we examined the potential for these epigenetic conflicts by focusing on three TE families in maize -Helitrons, Pack-MULEs and Sirevirus LTR retrotransposons. We documented 1,508 TEs with fragments captured from 2,019 donor genes and characterized the epigenetic profiles of both. Consistent with epigenetic conflict, donor genes mapped more siRNAs and were more methylated than 'free' genes that had no evidence of exon capture. However, these patterns differed between syntelog vs. transposed donor genes. Syntelog genes appeared to maintain function, consistent with moderation of the epigenetic response for important genes before reaching a deleterious threshold, while transposed genes bore the signature of silencing and potential pseudogenization. Intriguingly, transposed genes were overrepresented among donor genes, suggesting a link between capture and gene movement. We also investigated the potential for TEs to gain an advantage. TEs with captured fragments were older, mapped fewer siRNAs and had lower levels of methylation than 'free' TEs without gene fragments, but they showed no obvious evidence of increased copy numbers. Altogether, our results demonstrate that TE capture triggers an epigenetic conflict when genes are important, contrasting the loss of function for genes that are not under strong selective constraint. The evidence for an advantage to TEs is currently less obvious.

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Phylogenetic shifts in gene body methylation correlate with gene expression and reflect trait conservation

Cited by 7 publications

References 65 publications

Epigenetic inheritance mediates phenotypic diversity in natural populations

Epigenetic inheritance mediates phenotypic diversity in natural populations

Dnmt1a is essential for gene body methylation and the regulation of zygotic genome activation in the wasp

Gene capture by transposable elements leads to epigenetic conflict in maize

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