DNA Methylation and Gene Regulation in Honeybees: From Genome-Wide Analyses to Obligatory Epialleles
In contrast to heavily methylated mammalian genomes, invertebrate genomes are only sparsely methylated in a ‘mosaic’ fashion with the majority of methylated CpG dinucleotides found across gene bodies. Importantly, this gene body methylation is frequently associated with active transcription, and studies in the honeybee have shown that there are strong links between gene body methylation and alternative splicing. Additional work also highlights that obligatory methylated epialleles influence transcriptional changes in a context-specific manner. Here we discuss the current knowledge in this emerging field and highlight both similarities and differences between DNA methylation systems in mammals and invertebrates. Finally, we argue that the relationship between genetic variation, differential DNA methylation, other epigenetic modifications and the transcriptome must be further explored to fully understand the role of DNA methylation in converting genomic sequences into phenotypes.
KeywordsAnaplastic Lymphoma Kinase Transcriptional Change Royal Jelly Gene Body Methylation Invertebrate Genome
Anaplastic lymphoma kinase
Cytosine and guanine dinucleotide separated by one phosphate in DNA
microRNA small non-coding RNA of about 22 nucleotides
RNA-directed DNA methylation system
Ten-eleven translocation enzyme
- Ball MP, Li JB, Gao Y, Lee JH, LeProust EM, Park IH, et al. Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells (vol 27, pg 361, 2009). Nat Biotechnol. 2009;27(5):485.Google Scholar
- Capuano F, Mulleder M, Kok R, Blom HJ, Ralser M. Cytosine DNA methylation is found in Drosophila melanogaster but absent in Saccharomyces cerevisiae, Schizosaccharomyces pombe, and other yeast species. Anal Chem. 2014;86(8):3697–702. doi: 10.1021/ac500447w. Epub 2014 Mar 25.CrossRefPubMedPubMedCentralGoogle Scholar
- Holliday R, Pugh JE. DNA modification mechanisms for control of gene activity during development. Heredity. 1975;35(Aug):149.Google Scholar
- Kucharski R, Maleszka J, Maleszka R. A possible role of DNA methylation in functional divergence of a fast evolving duplicate gene encoding odorant binding protein 11 in the honeybee. Proc Biol Sci. 2016;283(1833):20160558. doi: 10.1098/rspb.2016.0558.
- Kulis M, Queiros AC, Beekman R, Martin-Subero JI. Intragenic DNA methylation in transcriptional regulation, normal differentiation and cancer. Bba-Gene Regul Mech. 2013;1829(11):1161–74.Google Scholar
- Maleszka R. Epigenetic code and insect behavioural plasticity. Curr Opin Insect Sci. 2016;15:45–52. doi: 10.1016/j.cois.2016.03.003.
- Waddington CH. The strategy of the genes. A discussion of some aspects of theoretical biology. London: George Allen & Unwin; 1957. p. 1957.Google Scholar
- Wojciechowski M, Rafalski D, Kucharski R, Misztal K, Maleszka J, Bochtler M, et al. Insights into DNA hydroxymethylation in the honeybee from in-depth analyses of TET dioxygenase. Open Biol. 2014;4(8). doi:Unsp 140110.Google Scholar
- Xiang H, Zhu JD, Chen QA, Dai FY, Li X, Li MW, et al. Single base-resolution methylome of the silkworm reveals a sparse epigenomic map (vol 28, pg 516, 2010). Nat Biotechnol. 2010;28(7):756.Google Scholar