The symbiont Wolbachia alleviates pesticide susceptibility in the two-spotted spider mite Tetranychus urticae through enhanced host detoxification pathways.

The two-spotted spider mite (Tetranychus urticae) is one of the most well-known pesticide-resistant agricultural pests, with resistance often attributed to changes such as target-site mutations and detoxification activation. Recent studies show that pesticide resistance can also be influenced by symbionts, but their involvement in this process in spider mites remains uncertain. Here, we found that infection with Wolbachia, a well-known bacterial reproductive manipulator, significantly increased mite survival after exposure to the insecticides abamectin, cyflumetofen, and pyridaben. Wolbachia-infected (WI) mites showed higher expression of detoxification genes such as P450, glutathione-S-transferase (GST), ABC transporters, and carboxyl/cholinesterases. RNA interference experiments confirmed the role of the two above-mentioned detoxification genes, TuCYP392D2 and TuGSTd05, in pesticide resistance. Increased GST activities were also observed in abamectin-treated WI mites. In addition, when wild populations were treated with abamectin, WI mites generally showed better survival than uninfected mites. However, genetically homogeneous mites with different Wolbachia strains showed similar survival. Finally, abamectin treatment increased Wolbachia abundance without altering the mite's bacterial community. This finding highlights the role of Wolbachia in orchestrating pesticide resistance by modulating host detoxification. By unraveling the intricate interplay between symbionts and pesticide resistance, our study lays the groundwork for pioneering strategies to combat agricultural pests.

Wolbachia manipulates reproduction of spider mites by influencing herbivore salivary proteins.

BACKGROUND: The endosymbiont Wolbachia is known for manipulating host reproduction. Wolbachia also can affect host fitness by mediating interactions between plant and herbivores. However, it remains unclear whether saliva proteins are involved in this process. RESULTS: We found that Wolbachia infection decreased the number of deposited eggs but increased the egg hatching rate in the spider mite Tetranychus urticae Koch (Acari: Tetranychidae), a cosmopolitan pest that infects >1000 species of plants. Transcriptomic and proteomic analyses revealed that Wolbachia-infected mites upregulated the gene expression levels of many T. urticae salivary proteins including a cluster of Tetranychidae-specific, functionally uncharacterized SHOT1s (secreted host-responsive proteins of Tetranychidae). The SHOT1 genes were expressed more in the feeding stages (nymphs and adults) of mites than in eggs and highly enriched in the proterosomas. RNA interference experiments showed that knockdown of SHOT1s significantly decreased Wolbachia density, increased the number of deposited eggs and decreased the egg hatching rate. CONCLUSION: Together, these results indicate that SHOT1s are positively correlated with Wolbachia density and account for Wolbachia-mediated phenotypes. Our results provide new evidence that herbivore salivary proteins are related to Wolbachia-mediated manipulations of host performance on plants. © 2022 Society of Chemical Industry.

Rop plays conserved roles in the reproductive and digestive processes of spider mites.

Ras opposite (Rop) is known to play an essential role in regulating vesicle trafficking, including synaptic transmission and general secretion. The fundamental roles of Rop have been confirmed by the observation that null mutations in many organisms generate lethal phenotypes during embryogenesis. However, the effects of Rop during the postembryonic stages, especially in non-model organisms, remain largely unknown. Here, we provide new data that enhance our understanding of Rop's roles in the adults of multiple species of Tetranychus spider mites (Acari: Tetranychidae), a class of notorious agricultural pests. Our in silico and experimental evidence demonstrated that Rop is under purifying selection and is highly conserved in Tetranychus spp. RNA interference experiments showed that Rop is required for maintaining normal fecundity but has no significant effect on survival. We further demonstrate that knockdown of Rop darkens the body color of spider mites and blocks the excretion of fecal pellets, which is likely to be related to an abnormality in the excretion of food waste in the digestive system. Overall, our findings clarify novel functions of a vesicle trafficking-related gene in the adult stage of multiple Tetranychus species and highlight the need to evaluate the roles of essential genes in various organisms.

Similarities and spatial variations of bacterial and fungal communities in field rice planthopper (Hemiptera: Delphacidae) populations.

Rice planthoppers are notorious plant sap-feeding pests which cause serious damage. While several microbes in rice planthoppers have been broadly characterized, the abundance and diversity of bacteria and fungi in field planthoppers are largely unknown. This study investigated the bacterial and fungal community compositions of Chinese wild rice planthoppers Laodelphax striatellus and Sogatella furcifera using parallel 16S rRNA gene amplicon and internal transcribed space region sequencing. The bacteria varied significantly between the species and were partitioned significantly by sex, tissues and host environments in each species. The majority of bacteria were affiliated with the genera Wolbachia, Cardinium, Rickettsia and Pantoea. The abundance of Wolbachia was negatively correlated with that of Cardinium in both planthopper species. Compared with bacteria, the abundance and diversity of fungi did not differ between sexes but both were enriched in the gut. The bacterial community as a whole showed no significant correlation with the fungal community. The majority of fungi were related to Sarocladium, Alternaria, Malassezia, Aspergillus and Curvularia. A phylogenetic analysis revealed that these fungi were closely related to botanic symbionts or pathogens. Our results provide novel insights into the bacteria and fungi of rice planthoppers.