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

Keith D Harris,Assaf Zemach,Daniel Zilberman,James P B Lloyd,Katherine Domb

doi:10.1186/s13072-019-0307-4

Abstract

BackgroundDNA 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 DNA methylation in honey bee, a model organism for gene body methylation.ResultsOur data show that CG methylation in gene bodies globally fluctuates during honey bee development. However, these changes cause no gene expression alterations. Intriguingly, despite the global alterations, tissue-specific CG methylation patterns of complete genes or exons are rare, implying robust maintenance of genic methylation during development. Additionally, we show that CG methylation maintenance fluctuates in somatic cells, while reaching maximum fidelity in sperm cells. Finally, unlike universally present CG methylation, we discovered non-CG methylation specifically in bee heads that resembles such methylation in mammalian brain tissue.ConclusionsBased on these results, we propose that gene body CG methylation can oscillate during development if it is kept to a level adequate to preserve function. Additionally, our data suggest that heightened non-CG methylation is a conserved regulator of animal nervous systems.

Highlights

DNA methylation of active genes, known as gene body methylation, is found in many animal and plant genomes
DNA methylation is distinctly regulated in the soma and germline To explain the molecular mechanism of gene body methylation dynamics during honey bee development, we examined the expression of honey bee DNA methyltransferases
We demonstrate that honey bee DNA methylation is distinctly regulated in the soma and germline

Summary

Introduction

DNA methylation of active genes, known as gene body methylation, is found in many animal and plant genomes. In animals and flowering plants, gene body methylation is enriched in the exons of highly conserved genes that are ubiquitously and moderately transcribed, e.g. housekeeping genes that are constitutively expressed in all cell types and under diverse conditions [14,15,16,17,18,19,20,21,22,23,24,25,26,27,28] These associations suggest a similar biological function, and possibly a common evolutionary origin, for gene body methylation in animals and plants. Other findings, including the lack of gene body methylation in earlybranching land plants and the linkage of genic methylation with a plant-specific DNA methyltranferase, support a convergent evolutionary model, in which gene body methylation evolved separately in animals and plants [30,31,32,33]

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