Below a certain level, table salt (NaCl) is beneficial for animals whereas excessive salt is harmful. However, it remains unclear how low and high salt perceptions are differentially encoded. Here, we identified a salt taste coding mechanism in Drosophila melanogaster. Flies use distinct types of gustatory receptor neurons (GRNs) to respond to different concentrations of salt. We demonstrated that a member of the newly discovered ionotropic glutamate receptor (IR) family, IR76b, functioned in detection of low salt, and was a Na+ channel. Loss of IR76b selectively impaired the attractive pathway, leaving salt-aversive GRNs unaffected. Consequently, low salt became aversive. Our work demonstrated that the opposing behavioral responses to low and high salt were determined largely by an elegant bi-modal switch system operating in GRNs.

Five canonical tastes, bitter, sweet, umami (amino acid), salty and sour (acid) are detected by animals as diverse as fruit flies and humans, consistent with a near universal drive to consume fundamental nutrients and to avoid toxins or other harmful compounds. Surprisingly, despite this strong conservation of basic taste qualities between vertebrates and invertebrates, the receptors and signaling mechanisms that mediate taste in each are highly divergent. The identification over the last two decades of receptors and other molecules that mediate taste has led to stunning advances in our understanding of the basic mechanisms of transduction and coding of information by the gustatory systems of vertebrates and invertebrates. In this review, we discuss recent advances in taste research, mainly from the fly and mammalian systems, and we highlight principles that are common across species, despite stark differences in receptor types.

Summary Food texture has enormous affects on food preferences. However, the mechanosensory cells and key molecules responsible for sensing the physical properties of food are unknown. Here, we show that akin to mammals, the fruit fly, Drosophila melanogaster, prefers food with a specific hardness or viscosity. This food texture discrimination depends upon a previously unknown multidendritic (md-L) neuron, which extends elaborate dendritic arbors innervating the bases of taste hairs. The md-L neurons exhibit directional selectivity in response to mechanical stimuli. Moreover, these neurons orchestrate different feeding behaviors depending on the magnitude of the stimulus. We demonstrate that the single Drosophila transmembrane channel-like (TMC) is expressed in md-L neurons, where it is required for sensing two key textural features of food—hardness and viscosity. We propose that md-L neurons are long-sought-after mechanoreceptor cells through which food mechanics are perceived and encoded by a taste organ, and this sensation depends on TMC.

Animals tend to reject bitter foods. However, long-term exposure to some unpalatable tastants increases acceptance of the foods. Here, we showed that dietary exposure to the unappealing food but safe additive, camphor, caused the fruit fly, Drosophila melanogaster, to decrease camphor rejection. The TRPL cation channel was a direct target for camphor in gustatory receptor neurons (GRNs), and long-term feeding on a camphor diet led to reversible down-regulation of TRPL protein levels. The turnover of TRPL was controlled by an E3 ubiquitin ligase, Ube3a. The decline in TRPL levels and increased acceptance of camphor reversed after returning the flies long-term to a camphor-free diet. We propose that dynamic regulation of taste receptor levels by ubiquitin-mediated protein degradation comprises an important molecular mechanism that allows an animal to alter taste behavior in response to a changing food environment.