Genome-wide temperature-sensitivity of Polycomb group regulation and reduction thereof in temperate Drosophila melanogaster

Abstract

Epigenetic regulation varies with the environment. In the fruit fly Drosophila melanogaster, environmental temperature can affect chromatin-based gene regulation. Genes regulated by the Polycomb group (PcG) can vary in their transcriptional output in response to changes in temperature, which typically increases with decreasing temperature. Here, we studied temperature-sensitive expression of PcG target genes on a genome-wide scale, as well as temperature-sensitive enrichment of two histone modifications associated with the regulation of PcG target genes, H3K27me3 and H3K4me3. We investigated temperature-sensitivity in adult flies, and possible differences thereof between populations adapted to temperate and tropical climates. Compared to genes not targeted by the PcG, an elevated number of target genes showed higher expression at the lower temperature, as it is typically observed for PcG regulation. Many of the PcG target genes also exhibited temperature-sensitive H3K4me3 enrichment in the same direction, and the H3K4me3 temperature response correlated positively with that of expression. A small set of target sites also showed temperature-sensitive enrichment of H3K27me3, again with a higher proportion corresponding to increased transcriptional activation at the lower temperature. Overall, higher transcriptional activity at lower temperature was less pronounced in males compared to females, and in temperate compared to tropical flies. Possible trans- and cis-acting factors responsible for reduced expression plasticity in temperate flies were identified, including factors belonging to the Trithorax group (TrxG) and insulator binding proteins, respectively.

Polycomb group proteins confer robustness to aposematic coloration in the milkweed bug, Oncopeltus fasciatus

“…PcG-regulated genes have been shown to evolve through temperature-dependent selection. Studies of different D. melanogaster populations have demonstrated that the temperature sensitivity of PcG target genes has diverged between tropical and temperate regions with reduced plasticity found in populations from temperate regions [20,48]. In addition, variants of the PcG genes themselves have been shown to be under selection in northern temperate populations of D. melanogaster, leading to the evolution of thermal plasticity [21].…”

Diversification and recurrent adaptation of the synaptonemal complex inDrosophila

“…As the RNA-seq datasets came from different studies, we tested the possibility that the expression differences resulted from external factors like rearing conditions and examined SC expression from RNA-seq of studies where flies were reared in different environmental conditions. In the datasets examined [56][57][58], SC expression shows minimal change in different rearing temperature (Supplementary Figure 15). Additionally, drastic expression divergence of the germlines can be observed in RNA-seq datasets we generated of closely related species reared in the same controlled laboratory condition, including those in the immigrans group and the sister species D. Nevertheless, these expression patterns reveal that despite the essential roles in regulating crossovers, germline transcriptional regulation of many SC genes is highly labile and constantly evolving, echoing their protein and copy number evolution.…”