Pleiotropic fitness effects of a Drosophila odorant-binding protein

Abstract

Insect odorant-binding proteins (OBPs) are members of a rapidly evolving multigene family traditionally thought to facilitate chemosensation. However, studies on Drosophila have shown that members of this family have evolved functions beyond chemosensation, as evident from their expression in reproductive tissues and the brain. Previous studies implicated diverse functions of Obp56h, a member of the largest gene cluster of the D. melanogaster Obp repertoire. Here, we examined the effect of CRISPR/Cas9-mediated deletion of Obp56h on 2 fitness phenotypes, on resistance to starvation stress and heat stress, and on locomotion and sleep phenotypes. Obp56h-/- mutants show a strong sexually dimorphic effect on starvation stress survival, with females being more resistant to starvation stress than the control. In contrast, Obp56h-/- females, but not males, are highly sensitive to heat stress. Both sexes show changes in locomotion and sleep patterns. Transcriptional profiling of RNA from heads of Obp56h-/- flies and the wildtype control reveals differentially expressed genes, including gene products associated with antimicrobial immune responses and members of the Turandot family of stress-induced secreted peptides. In addition, differentially expressed genes of unknown function were identified in both sexes. Genes encoding components of the mitochondrial electron transport chain, cuticular proteins, gene products associated with regulation of feeding behavior (Lst and CCHa2), ribosomal proteins, lncRNAs, snoRNAs, tRNAs, and snRNAs show changes in transcript abundances in Obp56h-/- females. These differentially expressed genes are likely to contribute to Obp56h-mediated effects on the diverse phenotypes that arise upon deletion of this OBP.

Keywords: Obp56h; CRISPR-Cas9; RNA sequencing; chemosensation; fitness; heat stress; pleiotropy; sexual dimorphism; sleep; starvation resistance.