The morphology and molecular mechanisms of enhanced olfaction in the grain aphid Sitobion miscanthi

Winged aphids develop more sensitive olfaction than the wingless phenotype to identify potential habitat from afar. Two types of olfactory sensilla, primary rhinarium (PRh) and secondary rhinarium (SRh) are responsible for aphid olfactory perception, of which, SRh is involved in the perception of both E-β-farnesene (EBF) and plant volatiles. Odorant binding proteins (OBPs) play a vital role in the response of insect olfactory nerves located in the rhinarium to external odor stimuli. However, the role of SRhs in winged aphids have received little attention to date and the underlying mechanisms of how OBPs work for the olfactory enhancement in winged aphids are unclear. Here, we compared and analyzed the number of SRhs on the antennae of winged and wingless aphids in the grain aphid Sitobion miscanthi, then highly expressed OBPs in antennae of winged aphids were screened based on both transcriptomic and proteomic data and identified by parallel reaction monitoring parallel reaction monitoring (PRM). Furthermore, the affinity of highly expressed OBPs was tested. The results showed that winged aphids have more SRhs, and the three highly expressed OBPs, SmisOBP6/7/10, in winged antennae shared broad and overlapped ligands spectra with plant volatiles and pheromones. Furthermore, OBP9, as an OBP with high expression in antennae, not only binds EBF, but also shows extensive affinity to various ligand types. Our results highlight the importance of the higher number of SRhs as the morphological basis of enhanced olfactory perception in winged aphid and further indicates the involvement of OBP6/7/10 as the molecular support of this process.