Comparative Insights Into Detoxification, Regulation, and Evolution of Neonicotinoid Resistance in Three Planthoppers.

Abstract

Planthoppers, the brown planthopper (BPH, Nilaparvata lugens), white-backed planthopper (WBPH, Sogatella furcifera), and small BPH (SBPH, Laodelphax striatellus) are among the most destructive rice pests in Asia. Neonicotinoid insecticides, particularly imidacloprid, have been widely deployed for their control, but intensive use has driven rapid evolution of high-level resistance across multiple species and regions. Long-term monitoring reveals pronounced spatial and temporal variation in resistance levels, shaped by local selection pressure and seasonal migration dynamics. Resistance is predominantly mediated by metabolic detoxification, with cytochrome P450 monooxygenases (CYPs), especially CYP6ER1 in BPH and its orthologs in WBPH and SBPH playing a central role, as confirmed by RNAi, heterologous expression, and genome-editing studies. Carboxylesterases, glutathione S-transferases, UDP-glycosyltransferases, and ATP-binding cassette transporters contribute additional detoxification capacity, whereas target-site mutations in nicotinic acetylcholine receptors remain comparatively minor in field populations. Transcriptomic analyses reveal that regulatory networks, including CncC/MafK, HNF4, and MAPK signaling-govern CYP overexpression, with comparative evidence highlighting convergent evolution of detoxification pathways across species. This review synthesizes current knowledge on resistance monitoring, molecular mechanisms, and evolutionary dynamics of neonicotinoid resistance in rice planthoppers, with emphasis on the BPH-imidacloprid system and comparative insights from WBPH and SBPH. Implications for integrated resistance management and sustainable pest control, including RNAi-based approaches, are also discussed.