Molecular Basis of Alarm Pheromone Detection in Aphids

The sesquiterpene (E)-β-farnesene (EBF) is the alarm pheromone for many species of aphids [1]. When released from aphids attacked by parasitoids or predators, it alerts nearby conspecifics to escape by walking away and dropping off the host plant [2, 3]. The reception of alarm pheromone in aphids is accomplished through a highly sensitive chemosensory system. Although olfaction-related gene families including odorant receptors (ORs) and odorant-binding proteins (OBPs) have recently been identified from aphid genomes [4-6], the cellular and molecular mechanisms of EBF reception are still largely unknown. Here we demonstrate that ApisOR5, a member of the large superfamily of odorant receptors, is expressed in large placoid sensillum neurons on the sixth antennal segment and confers response to EBF when co-expressed with Orco, an obligate odorant receptor co-receptor, in parallel heterologous expression systems. In addition, the repellent behavior of Acyrthosiphon pisum to EBF disappears after knocking down ApisOR5 by RNAi as well as two A. pisum odorant-binding proteins known to bind EBF (ApisOBP3 and ApisOBP7). Furthermore, other odorants that can also activate ApisOR5, such as geranyl acetate, significantly repel A. pisum, as does EBF. Taken together, these data allow us to conclude that ApisOR5 is essential to EBF reception in A. pisum. The characterization of the EBF receptor allows high-throughput screening of aphid repellents, providing the necessary information to develop new strategies for aphid control.