The Drosophila IR20a Clade of Ionotropic Receptors Are Candidate Taste and Pheromone Receptors

Abstract

Insects use taste to evaluate food, hosts, and mates. Drosophila has many “orphan” taste neurons that express no known taste receptors. The Ionotropic Receptor (IR) superfamily is best known for its role in olfaction, but virtually nothing is known about a clade of ~35 members, the IR20a clade. Here, a comprehensive analysis of this clade reveals expression in all taste organs of the fly. Some members are expressed in orphan taste neurons, whereas others are coexpressed with bitter- or sugar-sensing Gustatory receptor (Gr) genes. Analysis of the closely related IR52c and IR52d genes reveals signatures of adaptive evolution, roles in male mating behavior, and sexually dimorphic expression in neurons of the male foreleg, which contacts females during courtship. These neurons are activated by conspecific females and contact a neural circuit for sexual behavior. Together, these results greatly expand the repertoire of candidate taste and pheromone receptors in the fly.

Candidate ionotropic taste receptors in the Drosophila larva

“…S3 F-H). It thus seems likely that IR47a-GAL4 labels nonneuronal support cells of the TO, but further analysis will be required to identify the labeled cell types definitively; interestingly, in the adult taste system, IR47a-GAL4 expression appears to be neuronal (17). We note that nonneuronal expression has also been found for a member of the DEG/EnaC family of channels in the adult taste system (26).…”

“…To maximize the reliability of our analysis, we have (i) used drivers that contain not only sequences 5′ to the IR genes but sequences 3′ to the IR genes as well, (ii) inserted most drivers into common positions in the genome via the ϕC31 system, and (iii) examined multiple insertions of almost all constructs. Efforts to confirm expression patterns by in situ hybridization were made for some genes using a variety of methods, including tyramide signal amplification, but were unsuccessful, presumably due to low expression levels (16,17).…”

“…Among 26 members of the IR20a clade analyzed, one gene, IR60b, is distinguished from all others by its rate of evolutionary change (17). Specifically, it exhibits a negative direction of selection value of −0.28 (P = 0.004), as measured by the McDonaldKreitman test (41,42).…”

“…Another clade of 35 IR genes, called the IR20a clade, was recently shown to be expressed in gustatory neurons of Drosophila adults (17). Analysis of GAL4 drivers of 28 genes of the clade revealed expression of 16 drivers in adult taste neurons, collectively representing all taste organs of the fly.…”

The role of the sugar receptor IR60b for Drosophila melanogaster: A hypothesis

“…In Drosophila, the gustatory receptors GR64a-f and GR5a are expressed in neurons in taste sensilla on the labial palp and legs and mediate the "sweet" perception of multiple sugars and promote feeding in hungry flies (Jiao, Moon & Montell, 2007;Dahanukar et al, 2007;Fujii et al, 2015), while Gr43a expressing neurons in the brain sense hemolymph fructose and regulate feeding in a satiationdependent manner (Miyamoto et al, 2012). In a recent paper, Joseph and colleagues (Joseph et al, 2017) have characterized an additional sugar receptor, IR60b (Koh et al, 2014). This receptor is expressed in neurons of the labral sense organ in the pharynx, where they have direct contact with ingested food.…”