Article

Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci U S A

Departments of Entomology and Plant Science, Center for Chemical Ecology, and Intercollege Program in Genetics, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA 16802.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 09/2013; 110(39). DOI: 10.1073/pnas.1308867110
Source: PubMed

ABSTRACT

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 decemlineata) larvae exploit bacteria in their oral secretions to suppress antiherbivore defenses in tomato (Solanum 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, Pseudomonas, 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.

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    • "Previous work has shown that feeding by insect herbivores that induce the SA pathway can increase the developmental rate of co-feeding chewing insects (Rodriguez-Saona et al. 2005;Soler et al. 2012), as well as the recruitment of herbivores' natural enemies, which often respond to herbivore-induced plant volatiles whose emission is regulated by JA (). Crosstalk between signalling pathways thus creates the potential for manipulation of plant defence responses by some herbivores, including whiteflies (Zarate et al. 2007;Chung et al. 2013;Zhang et al. 2013;Su et al. 2015a). However, other herbivores, including Tetranychus evansi (the red tomato spider mite), appear capable of suppressing both JA and SA defences simultaneously (Sarmento et al. 2011a). "
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    • "These findings underscore the complexity of the plant hormone-based mechanisms in the interaction between plant, nematodes, and different herbivores. Which substances or specific signalling pathways are responsible for these opposite results, and whether microorganisms in the saliva of the studied herbivores play a role in defence induction (Chung et al., 2013), needs further scrutiny. "
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