Intragenic DNA methylation regulates insect gene expression and reproduction through the MBD/Tip60 complex

Xu, Guanfeng; Lyu, Hao; Yi, Yangqin; Peng, Yuling; Feng, Qili; Song, Qisheng; Gong, Chengcheng; Peng, Xuezhen; Palli, Subba Reddy; Zheng, Sichun

doi:10.1016/j.isci.2021.102040

Cited by 33 publications

(59 citation statements)

References 38 publications

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“…Previous studies have also investigated the role of DNA methylation in female reproductive life history strategies. For instance, a recent study found that gene knockdown of Dnmt1 and methyl-DNA-binding protein 2/3 ( MBD2/3 ) - a gene involved in gene body methylation in insects - and methylation inhibition by 5-aza-2’-deoxycytidine (a pharmaceutical alternative to Zeb) impaired ovary development and reduced fecundity and hatch rates in developing silkworm ( Bombyx mori ), tobacco cutworm ( Spodoptera litura ) and migratory locust ( Locusta migratoria ), suggesting intragenic DNA methylation regulates insect reproduction [56]. Silencing the Dnmt1 associated protein 1 ( DMAP1 ) gene severely reduced fecundity and offspring survival in the harlequin ladybird ( Harmonia axyridis ), suggesting a role of the DNMT-DMAP1 complex in life history traits in H. axyridis [23].…”

Section: Discussionmentioning

confidence: 99%

“…These findings may contradict previous studies that suggest an additional role of DNA methylation enzymes in reproductive tissues and gametogenesis in insects. For instance, significantly greater Dnmt1 expression was found in the oviposited eggs compared to the whole body of female adult red flour beetles ( Tribolium castaneum ), an insect that lacks a methylated genome but expresses Dnmt1 [57] and in the ovaries compared to other tissues in developing Bombyx mori [56]. Similarly, in the milkweed bug, Dnmt1 may play a specific role in oogenesis and is not required for somatic cell function (Amukamara et al ., 2020).…”

Section: Discussionmentioning

confidence: 99%

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Epigenetic Control of Temperature-Dependent Female Reproductive Life History Trade-Offs in Seed Beetles, Callosobruchus maculatus

McCaw

Leonard

Stevenson

et al. 2021

Preprint

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Many species are threatened by climate change and must rapidly respond to survive changing environments. Epigenetic modifications, such as DNA methylation, can facilitate plastic responses by regulating gene expression in response to environmental cues. Understanding epigenetic responses is therefore essential for predicting species’ ability to rapidly adapt in the context of global environmental change. Here, we investigated the functional significance of DNA methylation on temperature-dependent life history in seed beetles, Callosobruchus maculatus. We assessed changes in DNA methyltransferase (Dnmt1 and Dnmt2) expression levels under ambient conditions and thermal stress, and reproductive performance following artificially-induced epimutation via 3-aminobenzamide (3AB) and Zebularine (Zeb), at a range of ambient and warmer temperatures over two generations. We found that Dnmt1 and Dnmt2 were greatly expressed in females, throughout the body, and exhibited temperature-dependence; in contrast, Dnmt expression was minimal in males. Epimutation led to shifts in female reproductive life history trade-off allocation, and differentially altered thermal optima of fecundity and offspring viability. This study revealed the optimal allocation strategy among these fitness components is temperature-dependent, and trade-offs become increasingly difficult to resolve epigenetically under more extreme warming. Results suggest that epigenetic mechanisms are strongly implicated in, and perhaps limiting of, invertebrate life history responses to temperature change. Further investigation will reveal targeted DNA methylation patterns and specific loci associated with temperature-dependent life history trade-offs in seed beetles and other invertebrates.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Epigenetic Control of Temperature-Dependent Female Reproductive Life History Trade-Offs in Seed Beetles, Callosobruchus maculatus

McCaw

Leonard

Stevenson

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…S3). Future work should test whether intron hypermethylation induces downregulation of transcripts enriched with intragenic enhancers and whether positive associations between intron DM and DE are attributable to MBD-binding at methylated gene bodies, promoting histone H3K27 acetylation and gene expression (Xu et al, 2021).…”

Section: Differential Methylation's Effect On Expression Depends On Chromatin State and Genicmentioning

confidence: 99%

“…Recent advances in invertebrate epigenomics suggest that intragenic DNA methylation is bound by methyl-DNA-binding domain protein 2/3, which recruits acetyltransferases to promote H3K27 acetylation and initiate transcriptional elongation (Xu et al, 2021). Non-competing hypotheses posit that GBM may correlate with gene expression because it supports sequence conservation and transcriptional homeostasis.…”

Section: Relationships Between Dna Methylation Chromatin Accessibility and Genementioning

confidence: 99%

Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Bogan

Strader

Hofmann

2021

Preprint

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Epigenetic processes are proposed to contribute to phenotypic plasticity. In invertebrates, DNA methylation commonly varies across environments and can correlate or causally associate with phenotype, but its role in transcriptional responses to the environment remains unclear. Maternal environments experienced by the sea urchin Strongylocentrotus purpuratus induce 3 - 6x greater differential CpG methylation in offspring larvae relative to larval developmental environments, suggesting a role for DNA methylation in transgenerational plasticity (TGP). However, a negligible association has been observed between differentially methylated and differentially expressed genes. What gene regulatory roles does invertebrate DNA methylation possess under environmental change, if any? We quantified DNA methylation and gene expression in S. purpuratus larvae exposed to different ecologically relevant conditions during gametogenesis (maternal conditioning) or embryogenesis (developmental conditioning). We modeled differential gene expression and differential splicing under maternal conditioning as functions of DNA methylation, incorporating variables for genomic feature and chromatin accessibility. We detected significant interactions between differential methylation, chromatin accessibility, and genic architecture associated with differential expression and splicing. Observed transcriptional responses to maternal conditioning were also 4 - 13x more likely when accounting for interactions between methylation and chromatin accessibility. Our results provide evidence that DNA methylation possesses multiple functional roles during TGP in S. purpuratus, but its effects are contingent upon other genomic and epigenomic states. Singularly unpredictive of transcription, DNA methylation is likely one cog in the epigenomic machinery contributing to environmental responses and phenotypic plasticity in S. purpuratus and other invertebrates.

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“…DNA methylation can serve to repress expression of a individual allele by preventing a transcription factor from binding to a promoter region (Drewell et al, 2012). It is also thought DNA methylation can signal the recruitment of histone modifications which result in heterochromatin formation, silencing the expression of all alleles within a region (Barlow, 2011;Xu et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Caste- and sex-specific DNA methylation in a bumblebee is associated with codon degeneracy

Marshall

Nicholas

Zweden

et al. 2021

Preprint

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Genomic imprinting is defined as parent-of-origin allele-specific expression. In order for genes to be expressed in this manner an `imprinting' mark must be present to distinguish the parental alleles within the genome. In mammals imprinted genes are primarily associated with DNA methylation. Genes exhibiting parent-of-origin expression have recently been identified in two species of Hymenoptera with functional DNA methylation systems; Apis mellifera and Bombus terrestris. We carried out whole genome bisulfite sequencing of parents and offspring from reciprocal crosses of two B. terrestris subspecies in order to identify parent-of-origin DNA methylation. We were unable to survey a large enough proportion of the genome to draw a conclusion on the presence of parent-of-origin DNA methylation however we were able to characterise the sex- and caste-specific methylomes of B. terrestris for the first time. We find males differ significantly to the two female castes, with differentially methylated genes involved in many histone modification related processes. We also analysed previously generated honeybee whole genome bisulfite data to see if genes previously identified as showing parent-of-origin DNA methylation in the honeybee show consistent allele-specific methylation in independent data sets. We have identified a core set of 12 genes in female castes which may be used for future experimental manipulation to explore the functional role of parent-of-origin DNA methylation in the honeybee. Finally, we have also identified allele-specific DNA methylation in honeybee male thorax tissue which suggests a role for DNA methylation in ploidy compensation in this species.

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Intragenic DNA methylation regulates insect gene expression and reproduction through the MBD/Tip60 complex

Cited by 33 publications

References 38 publications

Epigenetic Control of Temperature-Dependent Female Reproductive Life History Trade-Offs in Seed Beetles, Callosobruchus maculatus

Epigenetic Control of Temperature-Dependent Female Reproductive Life History Trade-Offs in Seed Beetles, Callosobruchus maculatus

Gene regulation by DNA methylation is contingent on chromatin accessibility during transgenerational plasticity in the purple sea urchin

Caste- and sex-specific DNA methylation in a bumblebee is associated with codon degeneracy

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