Multi-functional roles of an antenna-specific odorant binding protein in Leptinotarsa decemlineata

Colorado potato beetle (CPB) is a notorious agricultural pest that is a specialist of solanaceous crops, causing millions in damage globally. A critical component to the prolificity of CPB is their ability to selectively locate their host through the detection of key chemical cues. Antennae are the primary olfactory organs, finely tuned to capturing airborne molecules, yet equally vulnerable to toxic or excess ligand in the sensillar lymph. Odorant binding proteins (OBPs) are the primary mediators connecting the external environment with insect olfactory receptors, potentially modulating the interaction of xenobiotics with the central nervous system. Here, we identified a highly expressed antennal-specific OBP in neonicotinoid resistant adult male CPB through our previous transcriptomic studies. To assess the affinity of this OBP towards various host plant compounds and pesticides, we performed competitive displacement fluorescence binding assays. Assay results revealed that this OBP binds to a wide range of plant volatiles and pesticides. Next, we used RNA interference combined with behavioral, electrophysiological, and toxicological bioassays to investigate the role of this OBP towards host location and pesticide resistance. We found that this OBP aids in host plant location by detecting stress-induced host plant volatiles and affects the susceptibility of adult male CPBs to imidacloprid. Our study is the first to functionally characterize an OBP of CPB in host location and insecticide resistance. Our findings provide insight into a key molecular factor involved in CPB’s response to environmental challenges and stressors, suggesting a potential link between insect adaptation to xenobiotics and olfactory processing.