Lineage and Parent-of-Origin Effects in DNA Methylation of Honey Bees (Apis mellifera) Revealed by Reciprocal Crosses and Whole-Genome Bisulfite Sequencing

Wu, Xin; Galbraith, David A.; Chatterjee, Paramita; Jeong, Hyeonsoo; Grozinger, Christina M.; Yi, Soojin V.

doi:10.1093/gbe/evaa133

Cited by 18 publications

(47 citation statements)

References 55 publications

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“…In contrast to our findings, two previous studies have suggested that honey bee workers kept under different social conditions exhibit a low number of DMRs, and that these are associated with differential gene expression (15,17). A plausible explanation (32,39) for these contrasting results is that previously-observed differences in the methylomes of honey bee workers in response to divergent social stimuli arose as an artifact of genotype-associated methylation variants (33). Indeed, when the colony genetic background was standardized, no differences were found between the methylomes of newly-emerged queens and newly-emerged workers (15).…”

Section: Discussioncontrasting

confidence: 99%

“…Therefore, these data provide strong support for the hypothesis that intragenic CpG methylation is not a driver of gene expression reprograming in the brain and ovary of young honey bees. This result is actually in line with and likely generalizable for other social insects (31,32,34,41,43,44,58).…”

Section: Discussionsupporting

confidence: 87%

“…More recent studies, however, now cast doubt on the role of gene body DNA methylation as a flexible regulator of gene expression in social insects, and an emerging consensus is that DNA methylation is genotype-specific (30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41). For example, a reanalysis of the Dnmt3 knockdown data of Li-Byarlay et al (2013) suggested that the original analysis had overestimated the number of regulated genes, and that the Dnmt3 knockdown had in fact only a minor effect on the honey bee gene body methylation pattern, and hence, on gene expression (37).…”

Section: Introductionmentioning

confidence: 99%

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

Junior

Yagound

Ronai

et al. 2021

Preprint

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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.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussionsupporting

confidence: 87%

Section: Introductionmentioning

confidence: 99%

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

Junior

Yagound

Ronai

et al. 2021

Preprint

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“…The epigenetic mechanisms that mediate PSGE in honey bees remains to be determined (Galbraith, Yi, et al, 2016). While there is evidence for parent‐specific gene methylation in honey bee workers, this variation in methylation does not correlate with parent‐specific gene expression patterns (Wu et al, 2020). Similar results were obtained in bumble bees (Marshall, Jones, et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…In honey bees, there have been no studies evaluating if PSGE patterns are conserved across tissues, and thus it is unclear how plastic these systems are. Furthermore, DNA methylation patterns are not significantly associated with transcription (Galbraith et al, 2015), and there is no association of parent‐specific DNA methylation patterns with parent‐specific gene expression (Wu et al, 2020). Thus, the epigenetic mechanism underlying these differences in allelic expression also remains to be determined.…”

Section: Introductionmentioning

confidence: 99%

Tissue‐specific transcription patterns support the kinship theory of intragenomic conflict in honey bees (Apis mellifera)

Galbraith

Grozinger

2021

Molecular Ecology

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Kin selection may act differently on genes inherited from parents (matrigenes and patrigenes), resulting in intragenomic conflict. This conflict can be observed as differential expression of matrigenes and patrigenes, or parent‐specific gene expression (PSGE). In honey bees (Apis mellifera), intragenomic conflict is hypothesized to occur in multiple social contexts. Previously, we found that patrigene‐biased expression in reproductive tissues was associated with increased reproductive potential in worker honey bees, consistent with the prediction that patrigenes are selected to promote selfish behaviour in this context. Here, we examined brain gene expression patterns to determine if PSGE is also found in other tissues. As before, the number of transcripts showing patrigene expression bias was significantly greater in the brains of reproductive vs. sterile workers, while the number of matrigene‐biased transcripts was not significantly different. Twelve transcripts out of the 374 showing PSGE in either tissue showed PSGE in both brain and reproductive tissues; this overlap was significantly greater than expected by chance. However, the majority of transcripts show PSGE only in one tissue, suggesting the epigenetic mechanisms mediating PSGE exhibit plasticity between tissues. There was no significant overlap between transcripts that showed PSGE and transcripts that were significantly differentially expressed. Weighted gene correlation network analysis identified modules which were significantly enriched in both types of transcripts, suggesting that these genes may influence each other through gene networks. Our results provide further support for the kin selection theory of intragenomic conflict, and provide valuable insights into the mechanisms which may mediate this process.

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DNA methylation is associated with codon degeneracy in a species of bumblebee

et al. 2023

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Social insects display extreme phenotypic differences between sexes and castes even though the underlying genome can be almost identical. Epigenetic processes have been proposed as a possible mechanism for mediating these phenotypic differences. Using whole genome bisulfite sequencing of queens, males, and reproductive female workers we have characterised the sex- and caste-specific methylome of the bumblebee Bombus terrestris. We have identified a potential role for DNA methylation in histone modification processes which may influence sex and caste phenotypic differences. We also find differentially methylated genes generally show low levels of DNA methylation which may suggest a separate function for lowly methylated genes in mediating transcriptional plasticity, unlike highly methylated genes which are usually involved in housekeeping functions. We also examined the relationship between the underlying genome and the methylome using whole genome re-sequencing of the same queens and males. We find DNA methylation is enriched at zero-fold degenerate sites. We suggest DNA methylation may be acting as a targeted mutagen at these sites, providing substrate for selection via non-synonymous changes in the underlying genome. However, we did not see any relationship between DNA methylation and rates of positive selection in our samples. In order to fully assess a possible role for DNA methylation in adaptive processes a specifically designed study using natural population data is needed.

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Lineage and Parent-of-Origin Effects in DNA Methylation of Honey Bees (Apis mellifera) Revealed by Reciprocal Crosses and Whole-Genome Bisulfite Sequencing

Cited by 18 publications

References 55 publications

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

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

Tissue‐specific transcription patterns support the kinship theory of intragenomic conflict in honey bees (Apis mellifera)

DNA methylation is associated with codon degeneracy in a species of bumblebee

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