Drosophila Sugar Receptors in Sweet Taste Perception, Olfaction, and Internal Nutrient Sensing

Abstract

SUMMARY Identification of nutritious compounds is dependent on expression of specific taste receptors in appropriate taste cell types [1]. In contrast to mammals, which rely on a single, broadly tuned heterodimeric sugar receptor [2], the Drosophila genome harbors a small subfamily of eight, closely related gustatory receptor (Gr) genes, Gr5a, Gr61a and Gr64a-f, of which three have been proposed to mediate sweet taste [3-6]. However, expression and function of several of these putative sugar Gr genes are not known. Here we present a comprehensive expression and functional analysis using GrLEXA/GAL4 alleles that were generated through homologous recombination. We show that sugar Gr genes are expressed in a combinatorial manner to yield at least eight sets of sweet sensing neurons. Behavioral investigations show that most sugar Gr mutations affect taste responses to only a small number of sugars and that effective detection of most sugars is dependent on more than one Gr gene. Surprisingly, Gr64a, one of three Gr genes previously proposed to play a major role in sweet taste [3, 4], is not expressed in labellar taste neurons, and Gr64a mutant flies exhibit normal sugar responses elicited from the labellum. Our analysis provides a molecular rationale for distinct tuning profiles of sweet taste neurons, and it favors a model whereby all sugar Grs contribute to sweet taste. Furthermore, expression in olfactory organs and the brain implies novel roles for sugar Gr genes in olfaction and internal nutrient sensing, respectively. Thus, sugar receptors may contribute to feeding behavior via multiple sensory systems.

Chemicals and chemoreceptors: ecologically relevant signals driving behavior in Drosophila

“…Plus, a very recent study demonstrated the expression of three sugar GRs, GR5a, GR64a, and GR64f, in adult olfactory organs although their function in these cells has not been determined yet (Fujii et al, 2015) (Figure 1 and Table 1). …”

“…) Adult antenna and/or maxillary palps GR21a-GR63a heterodimer? Clyne, 2000;Dunipace et al, 2001;Scott et al, 2001;Bray and Amrein, 2003;Colomb et al, 2007;Jones et al, 2007;Kwon et al, 2007Kwon et al, , 2011Miyamoto and Amrein, 2008;Thorne and Amrein, 2008;Montell, 2009;Lee et al, 2010;Park and Kwon, 2011;Liman et al, 2014;Ling et al, 2014;Fujii et al, 2015 Taste Adult labellum, internal taste organs, legs, and wing margin Heteromultimers with GR5a…”

“…Eight GRs, among them GR5a, are expressed in a combinatorial manner giving rise to a minimum of eight sets of sweet-sensing neurons in adult taste organs (Fujii et al, 2015). GR66a, GR93a, and GR33a appear to be coexpressed in most if not all bitter-sensing GRNs in the labellum Moon et al, 2009); plus, GR33a is necessary in those GRNs for the response to all bitter compounds tested (Moon et al, 2009).…”

“…In this section we will discuss the ecological relevance of specific chemoreceptors related to behaviors such as food searching and the analysis of its composition, avoidance of toxic or bitter compounds, oviposition site selection, and the search for a sexual partner ( Table 2). Glucose, maltose, sucrose, trehalose GR5a, GR61a, and GR64a-f * Labellum, legs, and internal taste organs Attraction Chyb et al, 2003;Thorne et al, 2004;Wang et al, 2004;Dahanukar et al, 2007;Jiao et al, 2007Jiao et al, , 2008Slone et al, 2007;Fujii et al, 2015 BITTER OR TOXIC COMPOUNDS Caffeine GR66a, GR33a, and GR93a Labellum and legs ppk23-ppk25-ppk29…”

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).…”