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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.

Herbivores and plants have been engaged in a tight co-evolutionary arms race, and saliva played important roles in this process. Some herbivore-derived small molecules or proteins called herbivore-associated molecular patterns (HAMPs) can be recognized by plants and thus trigger plant immune responses. Another type of salivary proteins, called effectors, utilize various strategies to suppress plant defense responses to establish successful feeding. The tomato red spider mite Tetranychus evansi is a worldwide pest of Solanaceous crops and causes enormous economic damage in many regions of the world. During the feeding process, T. evansi secretes saliva into plant cells through cheliceral stylets. Secreted saliva plays crucial roles in modulating plant-mite interaction, such as effectors Te28 and Te84 (Villarroel et al., 2016). We previously identified 136 salivary proteins from T. evansi by transcriptome and LC-MS/MS analyses (Huang et al., 2018). However, the role of these salivary proteins in mite-plant interaction was unknown. Here, we identified a salivary protein involved in the mite-plant interaction (Cui et al., 2022). This protein encodes a protein disulfide isomerase (TePDI) and acts as a HAMP that triggers plant defenses by inducing ROS burst, callose deposition and plant defense-related genes in Nicotiana benthamiana. TePDI can be recognized by multiple Solanaceae plants such as tomato, pepper, and eggplant. TePDI-mediated cell death in N. benthamiana is dependent on the plant signaling molecules SGT1 (suppressor of the G2 allele of skp1) and HSP90 (heat shock protein 90). To better feed on plants, T. evansi inhibited TePDI-triggered cell death and plant defense responses by secreting effectors Te28 and Te84. Further analysis revealed that PDI from phylogenetically distinct herbivorous and non-herbivorous arthropods all triggered cell death and immune response in N. benthamiana. Moreover, silencing PDI gene in spider mites and whiteflies resulted in the reduced survival rate of both pests. Altogether, our study revealed that PDI is a double-edged sword. On the one hand, it is functionally conserved in herbivores and required for their survival; on the other hand, it is recognized by Solanaceae plants and enhances plant resistance against herbivores. Our findings indicate that plants utilize evolutionarily conserved HAMPs to activate plant defense and resist pest damage, providing 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.

Nine bioactive ochromycinone analogues were synthesized through two different types of routes. Some unexpected products were obtained in the photo-induced oxidation. The syntheses disclosed herein complement those in the literature and offer inexpensive access to many of the known intermediates involved, most of which were studied years ago in completely different contexts.