The interactions between insects and their bacterial symbionts are shaped by a variety of abiotic factors, including temperature. As global temperatures continue to break high records, a great deal of uncertainty surrounds how agriculturally important insect pests and their symbionts may be affected by elevated temperatures, and its implications for future pest management. In this study, we examine the role of bacterial symbionts in the brown planthopper Nilaparvata lugens response to insecticide (imidacloprid) under different temperature scenarios. Our results reveal that the bacterial symbionts orchestrate host detoxification metabolism via the CncC pathway to promote host insecticide resistance, whereby the symbiont-inducible CncC pathway acts as a signaling conduit between exogenous abiotic stimuli and host metabolism. However, this insect-bacterial partnership function is vulnerable to high temperature, which causes a significant decline in host-bacterial content. In particular, we have identified the temperature-sensitive Wolbachia as a candidate player in N. lugens detoxification metabolism. Wolbachia-dependent insecticide resistance was confirmed through a series of insecticide assays and experiments comparing Wolbachia-free and Wolbachia-infected N. lugens and also Drosophila melanogaster. Together, our research reveals elevated temperatures negatively impact insect-bacterial symbiosis, triggering adverse consequences on host response to insecticide (imidacloprid) and potentially other xenobiotics.

Microbiome-mediated insecticide resistance is an emerging phenomenon found in insect pests. However, microbiome composition can vary by host genotype and environmental factors, but how these variations may be associated with insecticide resistance phenotype remains unclear. In this study, we compared different field and laboratory strains of the brown planthopper Nilaparvata lugens in their microbiome composition, transcriptome, and insecticide resistance profiles to identify possible patterns of correlation. Our analysis reveals that the abundances of core bacterial symbionts are significantly correlated with the expression of several host detoxifying genes (especially NlCYP6ER1, a key gene previously shown involved in insecticides resistance). The expression levels of these detoxifying genes correlated with N. lugens insecticide susceptibility. Furthermore, we have identified several environmental abiotic factors, including temperature, precipitation, latitude, and longitude, as potential predictors of symbiont abundances associated with expression of key detoxifying genes, and correlated with insecticide susceptibility levels of N. lugens. These findings provide new insights into how microbiome-environment-host interactions may influence insecticide susceptibility, which will be helpful in guiding targeted microbial-based strategies for insecticide resistance management in the field.

Monitoring is an important component of insecticide resistance management. In this study, resistance monitoring was conducted on 18 field populations in China. The results showed that S. furcifera developed high levels of resistance to chlorpyrifos and buprofezin, and S. furcifera showed low to moderate levels of resistance to imidacloprid, thiamethoxam, dinotefuran, clothianidin, sulfoxaflor, isoprocarb and ethofenprox. Sogatella furcifera remained susceptible or low levels of resistance to nitenpyram. LC50 values of nitenpyram and dinotefuran, imidacloprid, thiamethoxam, clothianidin and chlorpyrifos exhibited significant correlations, as did those between dinotefuran and thiamethoxam, clothianidin, sulfoxaflor, imidacloprid, isoprocarb and buprofezin. Similarly, significant correlations were observed between thiamethoxam and clothianidin, sulfoxaflor and imidacloprid. In addition, the activity of EST in field populations of S. furcifera were significantly correlated with the LC50 values of nitenpyram, thiamethoxam and clothianidin. These results will help inform effective insecticide resistance management strategies to delay the development of insecticide resistance in S. furcifera.

BACKGROUND Previous studies have shown that fungicides have insecticidal activity that can potentially be used as an insecticide resistance management strategy in the brown planthopper Nilaparvata lugens (Stål). However, the mechanism that induces mortality of N. lugens remains elusive. RESULTS In the present study, the insecticidal activities of 14 fungicides against N. lugens were determined, of which tebuconazole had the highest insecticidal activity compared with the other fungicides. Furthermore, tebuconazole significantly inhibited the expression of the chitin synthase gene NlCHS1; the chitinase genes NlCht1, NlCht5, NlCht7, NlCht9, and NlCht10; and the β‐N‐acetylhexosaminidase genes NlHex3, NlHex4, NlHex5 and NlHex6; it significantly suppressed the expression of ecdysteroid biosynthetic genes as well, including SDR, CYP307A2, CYP307B1, CYP306A2, CYP302A1, CYP315A1 and CYP314A1 of N. lugens. Additionally, tebuconazole affected the diversity, structure, composition, and function of the symbiotic fungi of N. lugens, as well as the relative abundance of saprophytes and pathogens, suggesting that tebuconazole reshapes the diversity and function of symbiotic fungi of N. lugens. CONCLUSION Our findings illustrate the insecticidal mechanism of tebuconazole, possibly by inhibiting normal molting or disrupting microbial homeostasis in N. lugens, and provide an important rationale for developing novel insect management strategies to delay escalating insecticide resistance. © 2023 Society of Chemical Industry.