DNA methylation is not a driver of gene expression reprogramming in young honey bee workers

Abstract

Intragenic DNA methylation, also called gene body methylation, is an evolutionarily- conserved epigenetic mechanism in animals and plants. In social insects, gene body methylation is thought to contribute to behavioral plasticity, for example between foragers and nurse workers, by modulating gene expression. However, recent studies have suggested that the majority of DNA methylation is sequence-specific, and therefore cannot act as a flexible mediator between environmental cues and gene expression. To address this paradox, we examined whole-genome methylation patterns in the brains and ovaries of young honey bee workers that had been subjected to divergent social contexts: the presence or absence of the queen. Although these social contexts are known to bring about extreme changes in behavioral and reproductive traits through differential gene expression, we found no significant differences between the methylomes of workers from queenright and queenless colonies. In contrast, thousands of regions were differentially methylated between colonies, and these differences were not associated with differential gene expression in a subset of genes examined. Methylation patterns were highly similar between brain and ovary tissues and only differed in nine regions. These results strongly indicate that DNA methylation is not a driver of differential gene expression between tissues or behavioral morphs. Finally, despite the lack of difference in methylation patterns, queen presence affected the expression of all four DNA methyltransferase genes, suggesting that these enzymes have roles beyond DNA methylation. Therefore, the functional role of DNA methylation in social insect genomes remains an open question.

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

“…We then called allele-specific DNA methylation in independently generated honeybee female data sets (n = 33) spanning various tissues of both workers and queens from Cardoso-Júnior et al . (2021); Yi et al .…”

“…To confirm the consistency of parent-of-origin DNA methylation in independently generated honeybee WGBS data we used the R package DAMEfinder v.1.2.0 (Orjuela et al ., 2020) to identify allelespecific DNA methylation in samples from the following recent studies: Yagound et al . (2019, 2020); Cardoso-Júnior et al . (2021); Yi et al .…”

Tools and applications for integrative analysis of DNA methylation in social insects

“…As the genetic background of drone thorax and semen is identical and semi‐conserved in the daughter workers, hsmCpG sets are most similar within a patriline, but methylation level similarity goes with cellular type; see also the discussion in Soley (2021) and (Yagound et al, 2021). Exciting new technologies are now being explored to probe DNA methylation at cell‐specific resolution rather than the aggregate view of large sample BS‐seq studies, suggesting possibilities of finely dissecting patterns and levels of methylation under different conditions (Cardoso‐Júnior et al, 2021; Kucharski & Maleszka, 2020).…”

Sex-specific transcription and DNA methylation landscapes of the Asian citrus psyllid, a vector of huanglongbing pathogens

“…gene promoters, can suppress gene expression levels by a ecting transcription factor binding and recruitment of the transcription initiation complex, typically causing stable silencing. Whereas gene-body DNA methylation, as is found in insects is generally reported to be associated with elevated, stable gene expression (Cardoso-Júnior et al, 2021;Glastad et al, 2016;Libbrecht et al, 2016). This may attribute to the fact that DNA methylomes profiled to date in insects have retained CpG methylation within constitutivly expressed gene bodies, which is proposed to a ect gene expression through regulation of transcription elongation and alternative splicing (Bewick et al, 2017;Bonasio et al, 2012;Lewis et al, 2020;Lorincz et al, 2004).…”