Functional analysis of odorant-binding proteins for the parasitic host location to implicate convergent evolution between the grain aphid and its parasitoid Aphidius gifuensis

(E)-8-farnesene (EBF) is a typical and ecologically important infochemical in tri-trophic level interactions among plant-aphid-natural enemies. However, the molecular mechanisms by which parasitoids recognize and utilize EBF are unclear. In this study, we functionally characterized 8 AgifOBPs in Aphidifus gifuensis, one dominant endo-parasitoid of wheat aphid as well as peach aphid in China. Among which, AgifOBP6 was the only OBP upregulated by various doses of EBF, and it showed a strong binding affinity to EBF in vitro. The lack of homology between AgifOBP6 and EBF-binding proteins from aphids or from other aphid natural enemies supported that this was a convergent evolution among insects from different orders driven by EBF. Molecular docking of Agi-fOBP6 with EBF revealed key interacting residues and hydrophobic forces as the main forces. AgifOBP6 is widely expressed among various antennal sensilla. Furthermore, two bioassays indicated that trace EBF may promote the biological control efficiency of A. gifuensis, especially on winged aphids. In summary, this study reveals an OBP (AgifOBP6) that may play a leading role in aphid alarm pheromone detection by parasitoids and offers a new perspective on aphid biological control by using EBF. These results will improve our understanding of tri-trophic level interactions among plant-aphid-natural enemies.

Automated summary

This study identified an OBP called AgifOBP6, which plays a crucial role in detecting and utilizing EBF in tri-trophic level interactions among plants, aphids, and natural enemies. AgifOBP6 can recognize and bind to EBF, thereby enhancing the efficiency of parasitoids in controlling their hosts.