Pleiotropic functions of an antenna-specific odorant binding protein linking xenobiotic adaptation and olfaction in the Colorado potato beetle, Leptinotarsa decemlineata

Abstract

The Colorado potato beetle, Leptinotarsa decemlineata, is the primary defoliator of potatoes and is notorious for its robust capability to develop resistance to various insecticides used to control it. As the initial interface between the environment and the insect olfactory system, odorant binding proteins (OBPs) solubilize and transport hydrophobic odorant molecules from the sensillar lymph to olfactory receptors. Recently, evidence has suggested that OBPs may also sequester excess harmful molecules such as insecticides in the perireceptor space, preventing them from reaching vulnerable olfactory sensory neuronal dendrites. In this study, we identified an antenna-specific OBP (LdecOBP33) that is 2.5-fold higher expressed in a neonicotinoid resistant strain than the susceptible one. Competitive displacement fluorescence binding assays revealed that LdecOBP33 protein binds to a wide range of compounds including various plant volatiles and insecticides. Next, we used RNA interference to knock down LdecOBP33 and combined with toxicological bioassays, behavioral, and electrophysiological assays to investigate functions of LdecOBP33 in insecticide resistance and host location. We found that LdecOBP33 silencing increased male beetles susceptibility to imidacloprid, suggesting its role in insecticide resistance. Additionally, LdecOBP33 aids in host location through enhancing the detection of stress-induced potato plant volatiles, increasing the efficacy of CPB adult foraging. Taken together, our study is the first to functionally characterize an OBP in CPB linked to insecticide resistance and host location. Our findings provide insight into a key molecular factor involved in CPBs response to environmental challenges, suggesting a potential link between insect adaptation to xenobiotics and olfactory processing.