Attracted or repelled?--a matter of two neurons, one pheromone binding protein, and a chiral center

Two species of scarab beetles, the Osaka beetle (Anomala osakana) and the Japanese beetle (Popillia japonica), utilize the opposite enantiomers of japonilure, (Z)-5-(1-decenyl)oxacyclopentan-2-one, as their sex pheromones. Each species produces only one of the enantiomers that functions as its own sex pheromone and as a very strong behavioral antagonist for the other species. Using an integrated approach we tested whether the discrimination of these two opposite signals is due to selective filtering by pheromone binding proteins or whether it originates in the specificity of ligand-receptor interactions. We found that the antennae of each of these two scarab species contain only a single pheromone binding protein, which associates with both enantiomers to a similar extent. The single neuron recording technique, on the other hand, showed that both species possess olfactory receptor neurons, colocalized in one sensillum, extremely specific to either (R)- or (S)-japonilure. Therefore, pheromone binding proteins (PBPs) alone cannot perform the task of chiral discrimination; enantiomeric specificity must be achieved by the interaction of the pheromone or the appropriate ligand-PBP complex with membrane receptors.