Plant Insecticide L-Canavanine Repels Drosophila via the Insect Orphan GPCR DmX

Abstract

Author SummaryPlants evolve to fend off the insects that attack them, often by synthesizing compounds toxic to insects. In turn, insects develop strategies to avoid these plants or resist their toxins. Some plant toxins are nonprotein amino acids. For example, seeds from numerous legumes contain high amounts of l-canavanine, a nonprotein amino acid that is structurally related to l-arginine and is highly toxic to most insects. How insects can detect l-canavanine remains to be elucidated. Using pharmacology, genetics, and behavioral approaches, we show that flies sense l-canavanine using the receptor DmX, an orphan G-protein–coupled receptor that has diverged in its ligand binding pocket from metabotropic glutamate receptors. Disruption of the DmXR gene, called mangetout (mtt), suppresses the l-canavanine repellent effect. DmXR is expressed and required in aversive gustatory receptor neurons, where it triggers the premature retraction of the proboscis, thus leading to the end of food searching. Our results indicate a mechanism by which some insects may detect and avoid a plant toxin.