Two Antenna-Enriched Odorant Binding Proteins in Dioryctria abietella Tuned to General Odorants and Insecticides

SIMPLE SUMMARY: Dioryctria abietella (Lepidoptera: Pyralidae) is a destructive forest pest that feeds on the shoots and cones of Pinaceae plants. The reception of host volatiles and toxic compounds can be mediated via odorant binding proteins (OBPs) expressed in olfactory organs. Here, a number of DabiOBPs may be involved in reproduction, as indicated by the expression profiles. Further, DabiOBP5 and DabiOBP14 enriched in adult antennae could strongly interact with two plant volatiles and four insecticides. Of these, β-ionone derived from plant flowers possibly served as an feeding attractant of female moths, while a pear ester ethyl-(2E,4Z)-decadienoate identified as a non-host volatile may repel D. abietella. In addition, two DabiOBPs were possibly associated with insecticide resistance. Molecular simulations identified several key residues involved in ligand-binding, revealing different binding mechanisms of DabiOBP5 and/or DabiOBP14 with the best ligands. These findings provide potentially active compounds for the control of D. abietella and characterize the interaction mechanisms of two antennal DabiOBPs with plant odorants and insecticides. ABSTRACT: The management of forest pests has become a significant challenge, particularly for wood borers, because they spend most of the time in the trunks or cones. The coneworm, Dioryctria abietella, is a representative of cone borers as its larvae feed on the cones of Pinaceae plants. The molecular mechanisms underlying the interactions between this species and host plants or habitats can assist in developing strategies for pest control. In this study, we extended the expression profiles of 32 odorant binding proteins (OBPs) in the reproductive tissues of D. abietella, revealing the detectable transcription of 29 genes. Using two DabiOBPs highly expressed in antennae (DabiOBP5 and DabiOBP14) as targets, six compounds with high affinities (dissociation constants < 13 μM) were identified through a reverse chemical ecology strategy, including insecticides widely used for the control of lepidopteran pests. Of these compounds, a floral volatile β-ionone and a pear-produced ester ethyl-(2E,4Z)-decadienoate may serve as behaviorally active compounds in D. abietella. The strong binding of DabiOBPs to insecticides suggested their involvement in insecticide resistance, reflecting sophisticated detoxification mechanisms of this moth. In the molecular simulations, DabiOBP14 possessed stronger interactions with the six ligands compared to DabiOBP5, in which a few key residues within the binding pockets were involved in the formation of hydrogen bonds. This study provides some valuable reference active compounds for the development of lures or repellents in D. abietella and unravels the putative roles of two antenna-dominant DabiOBPs in the perception of plant-derived odorants and insecticides.