Comparative studies of genomic and epigenetic factors influencing transcriptional variation in two insect species

Different genes show different levels of expression variability. For example, highly expressed genes tend to exhibit less expression variability. Genes whose promoters have TATA box and initiator motifs tend to have increased expression variability. On the other hand, DNA methylation of transcriptional units, or gene body DNA methylation, is associated with reduced gene expression variability in many species. Interestingly, some insect lineages, most notably Diptera including the canonical model insect Drosophila melanogaster, have lost DNA methylation. Therefore, it is of interest to determine whether genomic features similarly influence gene expression variability in lineages with and without DNA methylation. We analyzed recently generated large-scale data sets in D. melanogaster and honey bee (Apis mellifera) to investigate these questions. Our analysis shows that increased gene expression levels are consistently associated with reduced expression variability in both species, while the presence of TATA box is consistently associated with increased gene expression variability. In contrast, initiator motifs and gene lengths have weak effects limited to some data sets. Importantly, we show that a sequence characteristics indicative of gene body DNA methylation is strongly and negatively associate with gene expression variability in honey bees, while it shows no such association in D. melanogaster. These results suggest the evolutionary loss of DNA methylation in some insect lineages has reshaped the molecular mechanisms concerning the regulation of gene expression variability.

Automated summary

Different genomic features have varying effects on gene expression variability. Highly expressed genes tend to have less expression variability, while genes with TATA box tend to have increased expression variability. DNA methylation of transcriptional units is associated with reduced gene expression variability, except in certain insect lineages like Drosophila melanogaster. Our analysis of large-scale data sets in D. melanogaster and honey bee shows that increased gene expression levels and the presence of TATA box consistently influence gene expression variability in both species, while gene body DNA methylation has a negative association with gene expression variability only in honey bees.