Two Odorant-Binding Proteins Mediate the Behavioural Response of Aphids to the Alarm Pheromone (E)-ß-farnesene and Structural Analogues

Abstract

BackgroundAphids are agricultural pests of great economical interest. Alternatives to insecticides, using semiochemicals, are of difficult applications. In fact, sex pheromones are of little use as aphids reproduce partenogenetically most of the time. Besides, the alarm pheromone, (E)-ß-farnesene for a great number of species, is difficult to synthesize and unstable in the environment. The search for novel semiochemicals to be used in population control can be efficiently approached through the study of the olfactory system at the biochemical level. Recently odorant-binding proteins (OBPs) have been shown to play a central role in olfactory recognition, thus becoming the target of choice for designing new semiochemicals.Methodology/Principal FindingsTo address the question of how the alarm message is recognised at the level of OBPs, we have tested 29 compounds, including (E)-ß-farnesene, in binding assays with 6 recombinant proteins and in behaviour experiments. We have found that good repellents bind OBP3 and/or OBP7, while non repellents present different spectra of binding. These results have been verified with two species of aphids, Acyrthosiphon pisum and Myzus persicae, both using (E)-ß-farnesene as the alarm pheromone.ConclusionsOur results represent further support to the idea (so far convincingly demonstrated only in Drosophila) that OBPs are involved in decoding the chemical information of odorants and pheromones, and for the first time provide such evidence in other insect species and using wild-type insects. Moreover, the data offer guidelines and protocols for the discovery of potential alarm pheromones, using ligand-binding assays as a preliminary screening before subjecting selected compounds to behaviour tests.

Crystal structures and binding dynamics of odorant-binding protein 3 from two aphid speciesMegoura viciaeandNasonovia ribisnigri

“…NribOBP3 has a K i value of 5.2 μM for Eβ f, 20.2 μM for (− )-α -pinene and 30.7 μM for β -pinene. Therefore, MvicOBP3 and NribOBP3 could be involved in detecting and recognising Eβ f, which is consistent with previous reports of other aphid OBP3s [2][3][4] . MvicOBP3 seems to have a stronger binding affinity to these semiochemicals than NribOBP3 in the fluorescent competitive binding assay relative to the binding of NPN (Supplementary Figure 5).…”

“…This includes the detection of alarm pheromones. Research on the pea aphid, Acyrthosiphon pisum, has shown that the recognition of the alarm pheromone (E)-β -farnesene (Eβ f), and structurally related molecules, is mediated by ApisOBP3 and ApisOBP7 [2][3][4] . Homologous genes to ApisOBP3 have also been identified in other aphid species 5,6 and in other insects such as the hoverfly, Episyrphus balteatus (EbalOBP3) 3 and the brown plant hopper, Nilaparvata lugens (NlugOBP3) 7 with these OBPs showing an apparent high affinity for Eβ f. Indeed it was suggested that E. balteatus uses Eβ f as a kairomone to locate its aphid prey 8 .…”

Reverse chemical ecology: Olfactory proteins from the giant panda and their interactions with putative pheromones and bamboo volatiles

“…This phenomenon has been previously reported and attributed to formation of micelles when the concentration of the ligand is higher than its critical micelle concentration. Such micelles can encapsulate molecules of 1-NPN, thus enhancing the emitted fluorescence (42,43).…”

In vitro cytotoxic, genotoxic, and oxidative effects of acyclic sesquiterpene farnesene

“…It is odoriferous, and terpene-like substances occur in other natural sources: the trail markers of red fire ants (Van der Meer et al, 1982), alarm pheromones of aphids (Sun et al, 2012), and even a defense substance of wild potato plants against aphids (Bruce et al, 2005). The limited number of recent investigations has revealed that FNS possesses a wide range of important biological activities such as antibacterial activity (Chehregani et al, 2010), antifungal activity (Al-Maskri et al, 2011), and free radical-scavenging activity (Sarikurkcu et al, 2013).…”