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DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development

ABSTRACT: DNA methylation of active genes, also known as gene body methylation, is found in many animal and plant genomes. Despite this, the transcriptional and developmental role of such methylation remains poorly understood. Here, we explore the dynamic range of gene body methylation and its association with transcription and splicing in honey bee, an organism that targets methylation specifically to gene bodies. Our data show that gene body methylation globally fluctuates during honey bee development, with relatively high CG methylation in the embryo and adult stages and lower methylation in the larvae. We did not find a significant correlation between developmentally associated genic methylation dynamics and gene expression profiles. Furthermore, most developmentally regulated gene expression alterations occur in unmethylated genes. Tissue-specific methylation patterns, either at the level of complete genes or exons, are rare, implying robust maintenance of gene body methylation throughout the honeybee life cycle. Additionally, we show that CG methylation maintenance fluctuates in somatic cells, while reaching maximum fidelity in sperm cells. Finally, we report a Dnmt3-associated non-CG methylation signal in the gene bodies of adult bee heads that resembles the methylation patterns of mammalian brain tissue. Based on these results, we suggest that honey bee DNA methylation is distinctly regulated in the soma and germline. In the germline, methylation is efficiently maintained to preserve methylation patterns across generations. In contrast, methylation can fluctuate in somatic cells with limited division potential, as long as overall methylation of exons and genes remains at an adequate functional level. Additionally, we propose that heightened non-CG methylation may be a conserved characteristic of animal nervous systems.

ORGANISM(S): Apis mellifera

PROVIDER: GSE116629 | GEO | 2019/10/01

REPOSITORIES: GEO

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Project description:In honey bees (Apis mellifera) the behaviorally and reproductively distinct queen and worker female castes derive from the same genome as a result of differential intake of royal jelly and are implemented in concert with DNA methylation. To determine if these very different diet-controlled phenotypes correlate with unique brain methylomes, we conducted a study to determine the methyl cytosine (mC) distribution in the brains of queens and workers at single-base-pair resolution using shotgun bisulfite sequencing technology. The whole-genome sequencing was validated by deep 454 sequencing of selected amplicons representing eight methylated genes. We found that nearly all mCs are located in CpG dinucleotides in the exons of 5,854 genes showing greater sequence conservation than non-methylated genes. Over 550 genes show significant methylation differences between queens and workers, revealing the intricate dynamics of methylation patterns. The distinctiveness of the differentially methylated genes is underscored by their intermediate CpG densities relative to drastically CpG-depleted methylated genes and to CpG-richer non-methylated genes. We find a strong correlation between methylation patterns and splicing sites including those that have the potential to generate alternative exons. We validate our genome-wide analyses by a detailed examination of two transcript variants encoded by one of the differentially methylated genes. The link between methylation and splicing is further supported by the differential methylation of genes belonging to the histone gene family. We propose that modulation of alternative splicing is one mechanism by which DNA methylation could be linked to gene regulation in the honey bee. Our study describes a level of molecular diversity previously unknown in honey bees that might be important for generating phenotypic flexibility not only during development but also in the adult post-mitotic brain. This study looked at the DNA methylation levels of queen and worker honeybees

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DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development

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