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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.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 infects1000 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.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.

Herbivore-associated molecular patterns (HAMPs) enable plants to recognize herbivores and may help plants adjust their defense responses. Here, we report on herbivore-induced changes in a protein disulfide isomerase (PDI) widely distributed across arthropods. PDI from the spider mite Tetranychus evansi (TePDI), a mesophyll-feeding agricultural pest worldwide, triggered immunity in multiple Solanaceae plants. TePDI-mediated cell death in Nicotiana benthamiana required the plant signaling proteins SGT1 (suppressor of the G2 allele of skp1) and HSP90 (heat shock protein 90), but was suppressed by spider mite effectors Te28 and Te84. Moreover, PDIs from phylogenetically distinct herbivorous and nonherbivorous arthropods triggered plant immunity. Finally, although PDI-induced plant defenses impaired the performance of spider mites on plants, RNAi experiments revealed that PDI genes are essential for the survival of mites and whiteflies. Our findings indicate that plants recognize evolutionarily conserved HAMPs to activate plant defense and resist pest damage, pointing to opportunities for broad-spectrum pest management.

Background Host adaptation is the primary determinant of insect diversification. However, knowledge of different host ranges in closely related species remains scarce. The brown planthopper (Nilaparvata lugens, BPH) and the small brown planthopper (Laodelphax striatellus, SBPH) are the most destructive insect pests within the family Delphacidae. These two species differ in their host range (SBPH can well colonize rice and wheat plants, whereas BPH survives on only rice plants), but the underlying mechanism of this difference remains unknown. High-throughput sequencing provides a powerful approach for analyzing the association between changes in gene expression and the physiological responses of insects. Therefore, gut transcriptomes were performed to elucidate the genes associated with host adaptation in planthoppers. The comparative analysis of planthopper responses to different diets will improve our knowledge of host adaptation regarding herbivorous insects. Results In the present study, we analyzed the change in gene expression of SBPHs that were transferred from rice plants to wheat plants over the short term (rSBPH vs tSBPH) or were colonized on wheat plants over the long term (rSBPH vs wSBPH). The results showed that the majority of differentially expressed genes in SBPH showed similar changes in expression for short-term transfer and long-term colonization. Based on a comparative analysis of BPH and SBPH after transfer, the genes associated with sugar transporters and heat-shock proteins showed similar variation. However, most of the genes were differentially regulated between the two species. The detoxification-related genes were upregulated in SBPH after transfer from the rice plants to the wheat plants, but these genes were downregulated in BPH under the same conditions. In contrast, ribosomal-related genes were downregulated in SBPH after transfer, but these genes were upregulated in BPH under the same conditions. Conclusions The results of this study provide evidence that host plants played a dominant role in shaping gene expression and that the low fitness of BPH on wheat plants might be determined within 24 h after transfer. This study deepens our understanding of different host ranges for the two planthopper species, which may provide a potential strategy for pest management.

The cytochrome P450 monooxygenase (P450) gene family has an important role in detoxifying host plant allelochemicals and pesticides. In this study, we screened differentially expressed genes of the small brown planthopper (Laodelphax striatellus, SBPHs) that were reared for more than ten generations on rice and wheat plants, and found that only a few P450s were associated with host adaptation. LsCYP4DE1, whose expression was 9.5-fold higher in the wheat-adapted SBPH (wSBPH) than in the rice-adapted SBPH (rSBPH), appeared to have an important role in the colonization of wheat plants. Knocking down the expression of LsCYP4DE1 led to increased mortality, as well as decreased performance of SBPHs reared on wheat. However, no significant difference was found in dsLsCYP4DE1-treated SBPHs on rice plants. In addition, LsCYP4DE1 was potentially associated with pesticide tolerance, and suppression of its expression led to increased sensitivity to the pesticide ethiprole. Our results revealed potential roles of LsCYP4DE1 in wheat adaptation and ethiprole tolerance, and provide useful information for pest management.

Wolbachia are intracellular bacteria that manipulate host reproduction by several mechanisms including cytoplasmic incompatibility (CI). However, the underlying mechanisms of Wolbachia-induced CI are not entirely clear. Here, we monitored the Wolbachia distribution in the male gonads of the small brown planthopper ( Laodelphax striatellus , SBPH) at different development stages, and investigated the influence of Wolbachia on male gonads by a quantitative proteomic analysis. A total of 276 differentially expressed proteins were identified, with the majority of them participating in metabolism, modification, and reproduction. Knocking down the expression of outer dense fiber protein (ODFP) and venom allergen 5-like (VA5L) showed decreased egg reproduction, and these two genes might be responsible for Wolbachia improved fecundity in infected L. striatellus; whereas knocking down the expression of cytosol amino-peptidase-like (CAL) significantly decreased the egg hatch rate in Wolbachia-uninfected L. striatellus, but not in the Wolbachia-infected one. Considering that the mRNA/protein level of CAL was downregulated by Wolbachia infection and dsCAL treatment closely mimicked Wolbachia-induced CI, we presumed that CAL might be one of the factors determining the CI phenotype.

Extracellular DNA, released by damaged plant cells, acts as a damage-associated molecular pattern (DAMP). We demonstrated previously that the small brown planthopper (Laodelphax striatellus, SBPH) secreted DNase II when feeding on artificial diets. However, the function of DNase II in insect feeding remained elusive. The influences of DNase II on SBPHs and rice plants were investigated by suppressing expression of DNase II or by application of heterogeneously expressed DNase II. We demonstrated that DNase II is mainly expressed in the salivary gland and is responsible for DNA-degrading activity of saliva. Knocking down the expression of DNase II resulted in decreased performance of SBPH reared on rice plants. The dsDNase II-treated SBPH did not influenced jasmonic acid (JA), salicylic acid (SA), ethylene (ET) pathways, but elicited a higher level of H2 O2 and callose accumulation. Application of heterogeneously expressed DNase II in DNase II-deficient saliva slightly reduced the wound-induced defence response. We propose a DNase II-based invading model for SBPH feeding on host plants, and provide a potential target for pest management.