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.

Carboxylesterases (CarEs) represent one of the major detoxification enzyme families involved in insecticide resistance. However, the function of specific CarE genes in insecticide resistance is still unclear in the insect Nilaparvata lugens (Stål), a notorious rice crop pest in Asia. In this study, a total of 29 putative CarE genes in N. lugens were identified, and they were divided into seven clades; further, the β-esterase clade was significantly expanded. Tissue-specific expression analysis found that 17 CarE genes were abundantly distributed in the midgut and fat body, while 12 CarE genes were highly expressed in the head. The expression of most CarE genes was significantly induced in response to the challenge of nitenpyram, triflumezopyrim, chlorpyrifos, isoprocarb and etofenprox. Among these, the expression levels of NlCarE2, NlCarE4, NlCarE9, NlCarE17 and Nl-CarE24 were increased by each insecticide. Real-time quantitative polymerase chain reaction and RNA interference assays revealed the NlCarE1 gene to be a candidate gene mainly involved in nitenpyram resistance, while simultaneously silencing NlCarE1 and NlCarE19 produced a stronger effect than silencing either one individually, suggesting a cooperative relationship in resistance formation. These findings lay the foundation for further clarification of insecticide resistance mediated by CarE in N. lugens.

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The ATP-binding cassette (ABC) transporter superfamily is one of the largest groups of proteins and plays a non-negligible role in phase III of the detoxification process, which is highly involved in the response of insects to environmental stress (plant secondary metabolites and insecticides). In the present study, in Nilaparvata lugens, we identified 32 ABC transporters, which are grouped into eight subfamilies (ABCA–H) based on phylogenetic analysis. The temporal and spatial expression profiles suggested that the nymphal stages (1st–5th) and adult males showed similarity, which was different from eggs and adult females, and NlABCA1, NlABCA2, NlABCB6, NlABCD2, NlABCG4, NlABCG12, NlABCG15, and NlABCH1 were highly expressed in the midgut and Malpighian tubules. In addition, ABCG12, which belongs to the ABC transporter G subfamily, was significantly upregulated after exposure to sulfoxaflor, nitenpyram, clothianidin, etofenprox, chlorpyrifos, and isoprocarb. Moreover, verapamil significantly increased the sensitivity of N. lugens to nitenpyram, clothianidin, etofenprox, chlorpyrifos, and isoprocarb. These results provide a basis for further research on ABC transporters involved in detoxification in N. lugens, and for a more comprehensive understanding of the response of N. lugens to environmental stress.

BACKGROUND Nilaparvata lugens, a destructive rice pest in Asia, has developed resistance to many insecticides, including the neonicotinoid clothianidin. CYP6ER1 plays an important role in N. lugens resistant to clothianidin, but only limited information on the transcriptional regulation of CYP6ER1 overexpression in clothianidin resistance is available. RESULTS In this study, the transcription factor activator protein 1 (AP‐1) was found to be overexpressed in a clothianidin‐resistant strain of N. lugens and several field resistant populations. RNA interference‐mediated silencing of NlAP‐1 significantly decreased CYP6ER1 expression and increased the susceptibility of N. lugens to clothianidin. Additionally, NlAP‐1 was highly expressed in egg and adult stages, and in midguts, and NlAP‐1 was upregulated and induced to a greater extent in the clothianidin‐resistant strain after exposure to clothianidin. Finally, dual‐luciferase reporter assays confirmed the interaction between NlAP‐1 and the two predicted binding sites in the CYP6ER1 promoter. CONCLUSION NlAP‐1 bound the −1388 to −1208‐bp region of the CYP6ER1 promoter, enhancing its activity and then regulate the expression of CYP6ER1. These findings enhance our knowledge of the transcriptional regulation of the P450 genes that mediate insecticide resistance in insect pests. © 2021 Society of Chemical Industry.

Spodoptera frugiperda (J. E. Smith) is a worldwide economically important crop pest. Although the individuals of S. frugiperda that invaded China have been characterized as the corn strain, they also have the ability to damage other crops in China. The physiological and behavioral responses of S. frugiperda to different host plants are poorly understood. In the present study, we investigated the host plant preference, fitness costs, and differences in detoxification gene expression and microbiome composition between two S. frugiperda strains that fed on different crop plant diets. The results showed that S. frugiperda larvae exhibited no obvious preference for corn or rice, but significant suppression of development was observed in the rice-fed strain. In addition, the corn-fed strain showed higher insecticide tolerance and detoxification enzyme activities than the rice-fed strain. Moreover, multiple detoxification genes were upregulated in the corn-fed strain, and microbiome composition variation was observed between the two strains. Together, the results suggest that population-specific plasticity is related to host plant diets in S. frugiperda. These results provide a theoretical basis for the evolution of resistance differences in S. frugiperda and are helpful for designing resistance management strategies for S. frugiperda aimed at different crops.

The brown planthopper, Nilaparvata lugens, is one of the main insect pests of rice. The N. lugens gene NlCYP4CE1 encodes cytochrome P450 monooxygenase (P450), which is a key enzyme in the metabolism of the insecticide imidacloprid. Previous research has suggested that the expression of NlCYP4CE1 is induced by imidacloprid stress, but the effect of bacterial symbionts on its expression has not been determined. The results of this study show that exposure to subtoxic imidacloprid changed the structure of the bacterial symbiont community in N. lugens. Specifically, the total bacterial content increased, but the bacterial species diversity significantly decreased. Wolbachia accounted for the largest proportion of bacteria in N. lugens; its abundance significantly increased after subtoxic imidacloprid exposure. The transcript level of NlCYP4CE1 was significantly increased by imidacloprid, but this effect was significantly weakened after Wolbachia was cleared with tetracycline. This result suggests that Wolbachia enhances the expression of NlCYP4CE1 to promote the detoxification metabolic response to imidacloprid stress. Understanding the effect of bacterial symbionts on gene expression in the host provides a new perspective on interactions between insecticides and their target insect pests, and highlights that subtoxic imidacloprid exposure may raise the risk of insecticide resistance by altering the structure of bacterial symbiont communities.

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