Dinotefuran resistance in Nilaparvata lugens: resistance monitoring, inheritance, resistance mechanism and fitness costs

The brown planthopper (BPH), Nilaparvata lugens (Stal), is a major insect pest of rice in Asia and is mainly controlled with insecticides. Dinotefuran has been commercialized for control of N. lugens in China since 2013; however, the characteristics and mechanisms of resistance to dinotefuran are still unclear. Here, we conducted a long-term (from 2013 to 2021) and large geographical scale (11 provinces) resistance monitoring program for dinotefuran in the BPH in China. Before 2020, field populations of N. lugens have developed moderate resistance to dinotefuran, while since 2020, most field populations of N. lugens have developed high resistance. To develop a better resistance management strategy, a dinotefuran-resistant (Din-R) strain of N. lugens was selected in the laboratory to investigate the inheritance, possible mechanisms of resistance and potential fitness costs. This Din-R strain developed resistance to imidacloprid, nitenpyram and thiamethoxam. The dinotefuran resistance was controlled by multiple genes. RNA interference (RNAi)-mediated suppression of NlCYP6ER1, NlCYP6CS1 and NlCYP314A1 expression increased the susceptibility of N. lugens to dinotefuran. Transgenic lines of Drosophila melanogaster expressing NlCYP6ER1 or NlCYP314A1 were less susceptible to all four neonicotinoids. Furthermore, the Din-R strain had a relative fitness of 0.64 with a substantially decreased survival rate, emergence rate and fecundity. Collectively, our results showed that dinotefuran resistance was mediated by multiple CYP genes. The high expression of these genes was related to the cross-resistance of N. lugens to other neonicotinoids. This study provided valuable information for facilitating the development of neonicotinoids resistance management strategies.