A GPCR signaling pathway in insect odor detection

Abstract

Odor detection differs fundamentally in vertebrates, which use G protein-coupled receptors (GPCRs)1,2, and insects, which employ ion channels3,4. Here, we report the first evidence for a GPCR defining tuning properties of insect olfactory sensory neurons. Single-cell transcriptomics of the Drosophila melanogaster antenna identified selective expression of the G{gamma}30A subunit in acid-sensing Ir64a-DC4 neurons5,6. G{gamma}30A is essential for broadening responses to long-chain acids, acting with Gs, G{beta}13F, adenylate cyclase Ac13E and the Cngl channel. We further discovered that Cirl, a latrophilin-family GPCR7, is broadly-transcribed in the antenna but the protein is localized only in Ir64a-DC4 sensory cilia, dependent upon G{gamma}30A, but not Ir64a. Importantly, loss of Cirl also narrows Ir64a-DC4 tuning properties. Homologous neurons in Drosophila sechellia naturally exhibit narrow acid tuning, despite functional conservation of Ir64a; these differences correlate instead with lower expression of metabotropic components. Our findings reveal unexpected roles for GPCR/metabotropic signaling in olfactory detection and divergence in insects.