Abstract
Phenotypic differences between sexes are often mediated by differential expression and alternative splicing of genes. However, the mechanisms that regulate these expression and splicing patterns remain poorly understood. The mealybug, Planococcus citri, displays extreme sexual dimorphism and exhibits an unusual instance of sex-specific genomic imprinting, paternal genome elimination (PGE), in which the paternal chromosomes in males are highly condensed and eliminated from the sperm. Planococcus citri has no sex chromosomes and both sexual dimorphism and PGE are predicted to be under epigenetic control. We recently showed that P.citri females display a highly unusual DNA methylation profile for an insect species, with the presence of promoter methylation associated with lower levels of gene expression. Here, we therefore decided to explore genome-wide differences in DNA methylation between male and female P.citri using whole-genome bisulphite sequencing. We identified extreme differences in genome-wide levels and patterns between the sexes. Males display overall higher levels of DNA methylation which manifest as more uniform low levels across the genome. Whereas females display more targeted high levels of methylation. We suggest these unique sex-specific differences are due to chromosomal differences caused by PGE and may be linked to possible ploidy compensation. Using RNA-Seq, we identify extensive sex-specific gene expression and alternative splicing, but we find no correlation with cis-acting DNA methylation.
Highlights
Sexual dimorphism is widespread across sexually reproducing organisms
Supporting the idea that DNA methylation may be involved in sexual dimorphism and paternal genome elimination (PGE) in mealybugs and other scale insects, two recent studies have identified sex-biased expression of the DNA methyltransferase DNMT1 in adult Phenacoccus solenopsis (Omar et al, 2020) and Ericerus pela (Yang et al, 2015), with females showing considerably higher expression compared to males in both species
As we have previously shown using the female data in Lewis et al (2020), P. citri females have unusual patterns of DNA methylation compared to other insect species; we confirm that promoters, exons 1–3 and transposable elements (TEs) have significantly higher levels of DNA methylation compared to exons 4+ and introns (Figure 3c, Appendix S1: 1.0.8)
Summary
Sexual dimorphism is widespread across sexually reproducing organisms. Males and females can differ dramatically in morphology, behaviour and physiology. Supporting the idea that DNA methylation may be involved in sexual dimorphism and PGE in mealybugs and other scale insects, two recent studies have identified sex-biased expression of the DNA methyltransferase DNMT1 in adult Phenacoccus solenopsis (Omar et al, 2020) and Ericerus pela (Yang et al, 2015), with females showing considerably higher expression compared to males in both species. In order to identify sex-specific patterns of gene expression and clarify the role of DNA methylation in this process, we analyse both male and female P. citri methylomes and transcriptomes. This is the first genome-wide analysis of sex-specific gene expression and DNA methylation in scale insects. We find no relationship between differentially expressed genes and differentially methylated genes, indicating that cis-acting DNA methylation does not drive sex-specific gene expression in adult P. citri
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