The influence of Polycomb and Trithorax group function on the sexually dimorphic abdomen pigmentation of Drosophila melanogaster

Abstract Animal traits develop through intricate patterns of gene expression that are regulated at multiple levels. This regulation includes interactions between transcription factors and cis-regulatory element DNA sequences and the dynamic accessibility of cis-regulatory elements due to chromatin modifications and remodeling. Polycomb group and Trithorax group genes are evolutionarily conserved regulators of chromatin state. Although the Polycomb group and Trithorax group genes have well understood roles in developmental gene regulation, the extent to which these complexes contribute to trait evolution remains unclear. Here, we performed a genetic screen to understand how Polycomb group and Trithorax group genes shape the rapidly evolving gene regulatory network responsible for the dimorphic abdomen tergite pigmentation of Drosophila melanogaster fruit flies. A near-comprehensive screen of Trithorax group and Polycomb group genes was conducted using RNAi, and numerous genes were identified whose reduced expression caused alterations to tergite pigmentation. For the 8 most impactful genes, their roles in regulating this gene regulatory network were explored. We assessed their effects on several key transcription factors and downstream cis-regulatory elements that are responsible for the expression of the gene regulatory network's pigmentation enzyme genes. We show that multiple members of the Polycomb group and Trithorax group complexes are required for distinct tiers in the pigmentation gene regulatory network, suggesting potential points where responsive elements for different factors may have evolved. The results set the stage for future studies to identify the direct gene regulatory network targets of Polycomb group and Trithorax group complexes and how they have participated in the evolution of this gene regulatory network.