A pleiotropic chemoreceptor facilitates the functional coupling of pheromone production and perception

Abstract

Optimal mating decisions depend on the robust coupling of signal production and perception because independent changes in either could carry a fitness cost. However, since the perception and production of mating signals are often mediated by different tissues and cell types, the mechanisms that drive and maintain their coupling remain unknown for most animal species. Here, we show that in Drosophila, sensory perception and production of an inhibitory mating pheromone are co-regulated by Gr8a, a member of the Gustatory receptor gene family. Specifically, we found that the pleiotropic action of Gr8a independently regulates the perception of pheromones by the chemosensory systems of males and females, as well as their production in the fat body and oenocytes of males. These findings provide a relatively simple molecular explanation for how pleiotropic receptors maintain robust mating signaling systems at the population and species levels.

No functional contribution of the gustatory receptor, Gr64b, co-expressed in olfactory sensory neurons of Drosophila melanogaster

“…Recently, a role of Gr64 cluster genes was demonstrated in proteostasis and is crucial for the survival of ribosomal protein mutant epithelial cells in D. melanogaster (Baumgartner et al, 2021). Lastly, a pleiotropic role of GRs has been well documented in case of expression in the fly brain, gastrointestinal tract and reproductive sites (Park and Kwon, 2011; Miyamoto and Amrein, 2013; Vernier et al, 2022). Therefore, it can be hypothesized that Gr64b may not perform a chemosensory role but rather act as a GPCR involved in cellular functions when expressed in ab5B neurons.…”

“…The copyright holder for this preprint this version posted July 2, 2022. ; https://doi.org/10.1101/2022.06.29.498097 doi: bioRxiv preprint Watanabe et al, 2011;Lee et al, 2012;Freeman and Dahanukar, 2015;Fujii et al, 2015;Dweck and Carlson, 2020;Vernier et al, 2022). The first hint about non-canonical expression of GRs in the antenna of D. melanogaster came in the late 2000s, when two independent studies demonstrated that the perception of CO2 depends on Gr21a and Gr63a co-expressed in the ab1C neuron in the D. melanogaster antenna (Jones et al, 2007;Kwon et al, 2007).…”

“…Multiple studies have identified GRs that are required for tasting sweet and bitter compounds and describe diverse functional roles, such as inhibition of feeding and oviposition, inhibition of male to male courtship, etc. (Jiao et al, 2008; Moon et al, 2009; Watanabe et al, 2011; Lee et al, 2012; Freeman and Dahanukar, 2015; Fujii et al, 2015; Dweck and Carlson, 2020; Vernier et al, 2022). The first hint about non-canonical expression of GRs in the antenna of D. melanogaster came in the late 2000s, when two independent studies demonstrated that the perception of CO 2 depends on Gr21a and Gr63a co-expressed in the ab1C neuron in the D. melanogaster antenna (Jones et al, 2007; Kwon et al, 2007).…”