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Summary 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. [ABSTRACT FROM AUTHOR]

Numerous hematophagous insects are attracted to ammonia, a volatile released in human sweat and breath. 1–3 Low levels of ammonia also attract non-biting insects such as the genetic model organism Drosophila melanogaster and several species of agricultural pests. 4,5 Two families of ligand-gated ion channels function as olfactory receptors in insects, 6–10 and studies have linked ammonia sensitivity to a particular olfactory receptor in Drosophila. 5,11,12 Given the widespread importance of ammonia to insect behavior, it is surprising that the genomes of most insects lack an ortholog of this gene. 6 Here, we show that canonical olfactory receptors are not necessary for responses to ammonia in Drosophila. Instead, we demonstrate that a member of the ancient electrogenic ammonium transporter family, Amt, is likely a new type of olfactory receptor. We report two hitherto unidentified olfactory neuron populations that mediate neuronal and behavioral responses to ammonia in Drosophila. Their endogenous ammonia responses are lost in Amt mutant flies, and ectopic expression of either Drosophila or Anopheles Amt confers ammonia sensitivity. These results suggest that Amt is the first transporter known to function as an olfactory receptor in animals and that its function may be conserved across insect species. [Display omitted] • Ammonium transporters label previously uncharacterized neuron populations • These olfactory neurons selectively respond to ammonia • The Amt transporter acts as a non-canonical olfactory receptor in Drosophila • The function of Amt may be conserved across insect species Ammonia is an attractive odor for a wide variety of insects, including insect vectors of disease. Vulpe et al. identify a highly conserved ammonium transporter that functions as an olfactory receptor for ammonia. This transporter, Amt, is expressed in two hitherto uncharacterized neuronal populations in Drosophila. [ABSTRACT FROM AUTHOR]

Remarkable advances in our understanding of olfactory perception have been made in recent years, including the discovery of new mechanisms of olfactory signaling and new principles of olfactory processing. Here, we discuss the insight that has been gained into the receptors, cells, and circuits that underlie the sense of smell.