Abstract
DNA methylation is an epigenetic modification primarily responsible for individual phenotypic variation. This modification has been reported to play an important role in caste, brain plasticity, and body development in honeybees (Apis mellifera). Here, we report the DNA methylation profile of honeybee hypopharyngeal glands, from atrophy in winter to arousal in the following spring, through the use of whole-genome bisulfite sequencing. Consistent with previous studies in other Apis species, we found low methylation levels of the hypopharyngeal gland genome that were mostly of the CG type. Notably, we observed a strong preference for CpG methylation, which was localized in promoters and exon regions. This result further indicated that, in honeybees, DNA methylation may regulate gene expression by mediating alternative splicing, in addition to silencing gene in the promoter regions. After assessment by correlation analysis, we identified seven candidate proteins encoded by differentially methylated genes, including aristaless-related homeobox, forkhead box protein O, headcase, alpha-amylase, neural-cadherin, epidermal growth factor receptor, and aquaporin, which are reported to be involved in cell growth, proliferation, and differentiation. Hypomethylation followed by upregulated expression of these candidates suggested that DNA methylation may play significant roles in the activation of hypopharyngeal glands in overwintering honeybees. Overall, this study elucidates epigenetic modification differences in honeybee hypopharyngeal glands by comparing an inactive winter state to an aroused state in the following spring, which could provide further insight into the evolution of insect sociality and regulatory plasticity.
Highlights
Managing honeybee colonies throughout the winter has become a core agricultural issue in many countries and regions
Similar to that observed in other species, methylation in honeybees occurs in three sequence contexts: CG, CHG, and CHH
We found the overall levels of genome-wide methylated cytosine to be 67.65% CG, 4.11% CHG, and 28.23% CHH methylated C sites in the winter bee (WB) group, and 68.56% CG, 4.01% CHG, and 27.43% CHH methylated C sites in the spring bee (SB) group (Figure 2)
Summary
Managing honeybee colonies throughout the winter has become a core agricultural issue in many countries and regions. As insects of complex sociality, honeybees are capable of regulating their cluster temperature, normally maintaining a temperature ranging from 33 to 36°C in the presence of brood, even in the winter. Worker bees spend considerable physical energy synthesizing and secreting royal jelly to support the larvae and the queen in cold temperatures. This task is laborious, since the workers are simultaneously responsible for temperature maintenance. A fraction of eggs may fail to become larvae due to low temperatures, higher hatching rates are typically observed in larger colonies. The higher rate of energy consumption combined with lower production during winter results in maladapted reproductive behavior of queens during the winter
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