The full repertoire of Drosophila gustatory receptors for detecting an aversive compound

Abstract

The ability to detect toxic compounds in foods is essential for animal survival. However, the minimal subunit composition of gustatory receptors required for sensing aversive chemicals in Drosophila is unknown. Here we report that three gustatory receptors, GR8a, GR66a and GR98b function together in the detection of L-canavanine, a plant-derived insecticide. Ectopic co-expression of Gr8a and Gr98b in Gr66a-expressing, bitter-sensing gustatory receptor neurons (GRNs) confers responsiveness to L-canavanine. Furthermore, misexpression of all three Grs enables salt- or sweet-sensing GRNs to respond to L-canavanine. Introduction of these Grs in sweet-sensing GRNs switches L-canavanine from an aversive to an attractive compound. Co-expression of GR8a, GR66a and GR98b in Drosophila S2 cells induces an L-canavanine-activated nonselective cation conductance. We conclude that three GRs collaborate to produce a functional L-canavanine receptor. Thus, our results clarify the full set of GRs underlying the detection of a toxic tastant that drives avoidance behaviour in an insect.

Molecular and Cellular Organization of Taste Neurons in Adult Drosophila Pharynx

“…First, L-canavanine is known to activate bitter GRNs but it does not inhibit sweet GRNs (French et al, 2015, Jeong et al, 2013), which can otherwise confound interpretations of feeding assays using sugar/bitter mixtures. Second, L-canavanine is the only bitter compound for which a complete receptor repertoire has been described (Shim et al, 2015). A recent study reported a high affinity complex comprising Gr8a/Gr66a/Gr98b for detection of L-canavanine (Shim et al, 2015).…”

“…Second, L-canavanine is the only bitter compound for which a complete receptor repertoire has been described (Shim et al, 2015). A recent study reported a high affinity complex comprising Gr8a/Gr66a/Gr98b for detection of L-canavanine (Shim et al, 2015). Perusal of our receptor-to-neuron maps implicated a single Gr66a neuron, the V6 neuron in the VCSO, as a high affinity sensor of L-canavanine.…”

“…The previous study suggested that Gr8a and Gr66a together may be sufficient for a weak response to L-canavanine (Shim et al, 2015). We therefore tested the role of the Gr8a / Gr66a -labeled V7 neuron.…”

“…By contrast, some pharyngeal taste neurons express receptor combinations that are distinct from any that have been reported in other organs, leaving open questions about their functional roles. We validate the receptor-to-neuron maps derived from reporter gene expression by assessing roles of pharyngeal GRNs predicted to detect L-canavanine, a bitter tastant for which a complete receptor repertoire has been reported (Shim et al, 2015). Interestingly, a systematic activation analysis of different classes of pharyngeal taste neurons reveals functional differences between external and internal taste neurons for bitter avoidance and functional subdivision within pharyngeal sweet neurons for sweet acceptance.…”

Gustatory processing and taste memory inDrosophila

“…Sweet and bitter represent the best studied taste modalities, and a number of receptor– ligand pairs have been identified including Gr5a as a trehalose receptor and Gr66a as a receptor for caffeine (Dahanukar et al 2001, Jiao et al 2008, Weiss et al 2011, Miyamoto et al 2013, Ling et al 2014, Shim et al 2015). A subset of gustatory receptor neurons (GRNs) in the tarsi and mouth-parts express gustatory receptors for sugars, and activation of these neurons promotes feeding (Thorne et al 2004, Marella et al 2006).…”