Herbivores in disguise: the wolf in sheep’s clothing

Abstract: Herbivores possess diverse microbes in their digestive systems and these microbial symbionts may modify plant-insect interactions. However, the role of herbivore-associated microbes in manipulating plant defenses remains unclear. Here, we demonstrate that oral bacteria secreted by larvae of Colorado potato beetles (Leptinotarsa decemlineata) during herbivory suppress anti-herbivore defenses in tomato (Solanum lycopersicum). We found that antibiotic (AB)-treated larvae decreased JA-responsive anti-herbivore defenses, but increased SA-responsive gene expression. In SA-deficient NahG plants, this suppression was not observed, which suggests that suppression of JA-regulated defenses is dependent on the SA-signaling pathway. Application of bacteria isolated from OS of the larvae to wounded plants confirmed that three microbial symbionts, the genera Stenotrophomonas, Pseudomonas, and Enterobacter, are responsible for defense suppression. Additionally, re-inoculation of the suppressing bacteria to AB-treated larvae decreased plant defenses. Beetles benefit from down-regulated plant defenses through enhanced larval growth. Our findings indicate that the herbivore exploits oral bacteria as a decoy and thus plants incorrectly perceive the threat as microbial. By interfering with the normal perception of herbivory, beetles can evade anti-herbivore defenses of its host.