Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects

Abstract

Flying insects are well-known for airborne odor tracking, and evolved diverse chemoreceptors. While ionotropic receptors (IRs) are found across Protostomes, insect odorant receptors (ORs) have only been identified in winged insects. We therefore hypothesize that the unique signal transduction of ORs offers an advantage for odor localization in flight. Using Drosophila, we find expression and increased activity of the intracellular signaling protein, PKC, in antennal sensilla following odor stimulation. Odor stimulation also enhances phosphorylation of the OR coreceptor, Orco, in vitro, while site directed mutation of Orco or mutations in PKC subtypes reduces sensitivity and dynamic ranges of OR-expressing neurons in vivo, but not IRs. We ultimately show that these mutations reduce competence for odor localization of flies in flight. We conclude that intracellular regulation of OR sensitivity is necessary for efficient odor localization, which suggests a mechanistic advantage for the evolution of the OR complex in flying insects.