Abstract
Given the importance of DNA methylation in protection of the genome against transposable elements and transcriptional regulation in other taxonomic groups, the diversity in both levels and patterns of DNA methylation in the insects raises questions about its function and evolution. We show that the maintenance DNA methyltransferase, DNMT1, affects meiosis and is essential to fertility in milkweed bugs, Oncopeltus fasciatus, while DNA methylation is not required in somatic cells. Our results support the hypothesis that Dnmt1 is required for the transition of germ cells to gametes in O. fasciatus and that this function is conserved in male and female gametogenesis. They further suggest that DNMT1 has a function independent of DNA methylation in germ cells. Our results raise thequestion as to how a gene that is so critical to fitness across multiple insect species is able to diverge widely across the insect tree of life.
Highlights
Despite the apparent ubiquity of DNA methylation across the eukaryotic tree of life (Schmitz et al, 2019; Lewis et al, 2020), in the insects there is considerable variation both in the presence and extent of DNA methylation and even the presence and number of the DNA methyltransferases (Bewick et al, 2016; Lyko, 2018; Glastad et al, 2019)
The reduction of DNA methylation is an evolved difference rather than an experimental effect, but the results are similar to what we have observed in O. fasciatus; DNA methylation is not required for function of somatic cells, but downregulation of Dnmt1 expression leads to specific germ cell effects
Dnmt1 expression is required for germ cell development in both male and female O. fasciatus
Summary
Despite the apparent ubiquity of DNA methylation across the eukaryotic tree of life (Schmitz et al, 2019; Lewis et al, 2020), in the insects there is considerable variation both in the presence and extent of DNA methylation and even the presence and number of the DNA methyltransferases (Bewick et al, 2016; Lyko, 2018; Glastad et al, 2019). We observed apHH3 staining in spermatocysts (testis region III) at the border between primary and secondary spermatocytes in the control testis tubules in both third and fifth instar treated males. The testis tubules of males treated with ds-Dnmt in the fifth instar stage of development had a structure much more similar to control males (Figure 6D). Mitotic activity was apparent in the spermatogonia (Figure 6D arrowhead) and most testis tubules had evidence of mature sperm and apHH3 stained spermatocysts at the junction between primary and secondary spermatocytes (Figure 6D arrow) Unorganized spermatocysts below this junction were frequently observed, and ds-Dnmt males treated at the fifth instar had variable phenotypes posterior to the primary spermatocytes, presumably depending on when treatment occurred following the. Boule knockdown with RNAi showed the expected phenotype in males
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