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Lepidopterans commonly feed on plant material, being the most significant insect herbivores in nature. Despite plant resistance to herbivory, such as producing toxic secondary metabolites, herbivores have developed mechanisms encoded in their genomes to tolerate or detoxify plant defensive compounds. Recent studies also highlight the role of gut microbiota in mediating detoxification in herbivores; however, convincing evidence supporting the significant contribution of gut symbionts is rare in Lepidoptera. Here, we show that the growth of various lepidopteran species was inhibited by a mulberry-derived secondary metabolite, 1-deoxynojirimycin (DNJ); as expected, the specialist silkworm Bombyx mori grew well, but interestingly, gut microbiota of early-instar silkworms was affected by the DNJ level, and several bacterial species responded positively to enriched DNJ. Among these, a bacterial strain isolated from the silkworm gut (Pseudomonas fulva ZJU1) can degrade and utilize DNJ as the sole energy source, and after inoculation into nonspecialists (e.g., beet armyworm Spodoptera exigua), P. fulva ZJU1 increased host resistance to DNJ and significantly promoted growth. We used genomic and transcriptomic analyses to identify genes potentially involved in DNJ degradation, and CRISPR-Cas9- mediated mutagenesis verified the function of ilvB, a key binding protein, in metabolizing DNJ. Furthermore, the ilvB deletion mutant, exhibiting normal bacterial growth, could no longer enhance nonspecialist performance, supporting a role in DNJ degradation in vivo. Therefore, our study demonstrated causality between the gut microbiome and detoxification of plant chemical defense in Lepidoptera, facilitating a mechanistic understanding of host-microbe relationships across this complex, abundant insect group. [ABSTRACT FROM AUTHOR]

Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called "polydnaviruses." Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant-herbivore interactions than ever considered. [ABSTRACT FROM AUTHOR]

Induced plant defenses in response to herbivore attack are modulated by cross-talk between jasmonic acid (JA)- and salicylic acid (SA)-signaling pathways. Oral secretions from some insect herbivores contain effectors that overcome these antiherbivore defenses. Herbivores possess diverse microbes in their digestive systems and these microbial symbionts can modify plant-insect interactions; however, the specific role of herbivore-associated microbes in manipulating plant defenses remains unclear. Here, we demonstrate that Colorado potato beetle (Leptinotarsa decem-lineata) larvae exploit bacteria in their oral secretions to suppress antiherbivore defenses in tomato (Solarium lycopersicum). We found that antibiotic-untreated larvae decreased production of JA and JA-responsive antiherbivore defenses, but increased SA accumulation and SA-responsive gene expression. Beetles benefit from down-regulating plant defenses by exhibiting enhanced larval growth. In SA-deficient plants, suppression was not observed, indicating that suppression of JA-regulated defenses depends on the SA-signaling pathway. Applying bacteria isolated from larval oral secretions to wounded plants confirmed that three microbial symbionts belonging to the genera Stenotrophomonas, Pseudo-monas, and Enterobacter are responsible for defense suppression. Additionally, reinoculation of these bacteria to antibiotic-treated larvae restored their ability to suppress defenses. Flagellin isolated from Pseudomonas sp. was associated with defense suppression. Our findings show that the herbivore exploits symbiotic bacteria as a decoy to deceive plants into incorrectly perceiving the threat as microbial. By interfering with the normal perception of herbivory, beetles can evade antiherbivore defenses of its host. [ABSTRACT FROM AUTHOR]