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Gene body methylation suppresses intragenic transcription and permits epigenetic inheritance in a cnidarian

ABSTRACT: DNA methylation is traditionally associated with silencing, yet in invertebrates most methylation accumulates in actively transcribed gene bodies, posing a longstanding paradox. Gene body methylation (gbM) has been hypothesized to stabilize gene expression, suppress intragenic transcription, or mediate environmental responses, yet direct experimental evidence for its function remains limited. Here, we use the cnidarian Nematostella vectensis to demonstrate that loss of DNA methylation results in viable embryos with only mild effects on gene expression. Instead, methylation depletion leads to extensive aberrant accessibility and spurious transcriptional initiation, particularly associated to transposable elements within normally methylated gene bodies. This supports a model in which gbM suppresses cryptic regulatory activity in broadly transcribed regions. We further show that abnormal methylation patterns are partially restored in the germline, with recovery biased toward transcriptionally active regions and excluded from repressive chromatin. These epimutations are inherited into the next generation, revealing the absence of epigenetic reprogramming. Our findings uncover a conserved protective role for gbM, demonstrate its capacity for transgenerational inheritance, and highlight its potential as a regulatory substrate for natural selection.

ORGANISM(S): Nematostella vectensis

PROVIDER: GSE307384 | GEO | 2026/04/10

REPOSITORIES: GEO

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Project description:We utilized the Nematostella vectensis to quantify gene expression differences and loss during light:dark cycling and immediately after light cue removal through comparisons of 136 transcriptomes Organismal responses to light:dark cycles can result from two general processes: (i) direct response to light or (ii) a free-running rhythm (i.e., a circadian clock). Previous research in cnidarians has shown that candidate circadian clock genes have rhythmic expression in the presence of diel lighting, but these oscillations appear to be lost quickly after removal of the light cue. Here, we measure whole-organism gene expression changes in 136 transcriptomes of the sea anemone Nematostella vectensis, entrained to a light:dark environment and immediately following light cue removal to distinguish two broadly defined responses in cnidarians: light entrainment and circadian regulation. Direct light exposure resulted in significant differences in expression for hundreds of genes, including more than 200 genes with rhythmic, 24-hour periodicity. Removal of the lighting cue resulted in the loss of significant expression for 80% of these genes after one day, including most of the hypothesized cnidarian circadian genes. Further, 70% of these candidate genes were phase shifted. Most surprisingly, thousands of genes, some of which are involved in oxidative stress, DNA damage response, and chromatin modification, had significant differences in expression in the 24 hours following light removal, suggesting that loss of the entraining cue may induce a cellular stress response. Together, our findings suggest that a majority of genes with significant differences in expression for anemones cultured under diel lighting are largely driven by the primary photoresponse rather than a circadian clock when measured at the whole animal level. These results provide context for the evolution of cnidarian circadian biology and help to disassociate two commonly confounded factors driving oscillating phenotypes.

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Gene body methylation suppresses intragenic transcription and permits epigenetic inheritance in a cnidarian

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