Cytochrome P450 Drives Divergent Adaptation to Quercetin in Invasive and Native Fruit Borers

Abstract

Plant-herbivore coevolution drives insect adaptation. Cydia pomonella, an invasive fruit borer, adapts more slowly to quercetin than native Grapholita molesta, yet the molecular basis remains unclear. This study reveals their divergent quercetin adaptation mechanisms. Pre-invasion in northeastern China, C. pomonella likely encountered no host-defense pressure at 70.0 μg/g quercetin. Post-adaptation, both species enhanced quercetin metabolism compared to their non-adapted counterparts. AI-driven molecular modeling, RNAi, and in vitro metabolism studies showed G. molesta employed classical detoxifying CYP3 and CYP4 P450s for quercetin detoxification. Conversely, C. pomonella achieved adaptation by neofunctionalizing mitochondrial P450 genes. However, C. pomonella’s quercetin-adaptation P450s had lower quercetin metabolic capability than G. molesta’s. These findings suggest divergent adaptive strategies among species, with invasive species C. pomonella potentially employing mitochondrial P450 neofunctionalization for xenobiotic detoxification and host adaptation, facilitating invasion. These findings advance our comprehension of host adaptability and the intricate interspecific interactions between invasive and native pest species.