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


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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    ABSTRACT: Plants frequently engage in simultaneous interactions withdiverse classes of biotic antagonists. Differential induction ofplant defence pathways by these antagonists, and interactionsbetween pathways, can have important ecological implications; however, these effects are currently not well understood. We explored how Tomato yellow leaf curl virus (TYLCV) influenced the performance of its vector (Bemisia tabaci) and a non-vector herbivore (Tetranychus urticae) occurring separately or together on tomato plants (Solanum lycopersicum). TYLCV enhanced the performance of B. tabaci, although this effect was statistically significant only in the absence of T. urticae, which adversely affected B. tabaci performance regardless of infection status. In contrast, the performance of T. urticae was enhanced (only) by the combined presence of TYLCV and B. tabaci. Analyses of phytohormone levels and defence gene expression in wild-type tomatoes and various plant-defence mutants indicate that the enhancement of herbivore performance (for each species) entails the disruption of downstream defences in the jasmonic acid (JA) pathway. For T. urticae, this disruption appears to involve antagonistic effects of salicylic acid (SA), which is cumulatively induced to high levels by B. tabaci and TYLCV. In contrast, TYLCV was found to suppress JA-mediated responses to B. tabaci via mechanisms independent of SA.
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    • "This would suggest that the insect might distinguish between pathogenic and common non-pathogenic bacteria and does not upregulate its immune system in response to common phyllosphere bacteria. Such a distinction could be valuable as non-entomopathogenic bacteria acquired from plants, and those that colonise the insect digestive system, can play beneficial roles (Chu et al., 2013; Chung et al., 2013; Mason et al., 2014). Other non-entomopathogenic organisms are also found in the phyllosphere, such as yeasts and other fungi. "
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    ABSTRACT: 1. The aerial surface of plants is a habitat for large and diverse microbial communities; termed the phyllosphere. These microbes are unavoidably consumed by herbivores, and while the entomopathogens are well studied, the impact of non-pathogenic bacteria on herbivore life history is less clear. 2. Previous work has suggested that consumption of non-entomopathogenic bacteria induces a costly immune response that might decrease the risk of infection. However, we hypothesised that insect herbivores should be selective in how they respond to commonly encountered non-pathogenic bacteria on their host plants to avoid unnecessary and costly immune responses. 3. An ecologically realistic scenario was used in which we fed cabbage looper, Trichoplusia ni Hübner, larvae on cabbage or cucumber leaves treated with the common non-entomopathogenic phyllosphere bacteria, Pseudomonas fluorescens and P. syringae. Their constitutive immunity and resistance to a pathogenic bacterium (Bacillus thuringiensis; Bt) and a baculovirus (T. ni single nucleopolyhedrovirus) were then examined. 4. While feeding on bacteria-treated leaves reduced the growth rate and condition of T. ni, there was no effect on immunity (haemolymph antibacterial and phenoloxidase activities and haemocyte numbers). Phyllosphere bacteria weakly affected the resistance of T. ni to Bt but the direction of this effect was concentration dependent; resistance to the virus was unaffected. Host plant had an impact, with cucumber-fed larvae being more susceptible to Bt. 5. The lack of evidence for a costly immune response to non-entomopathogenic bacteria suggests that T. ni are probably adapted to consuming common phyllosphere bacteria, and highlights the importance of the evolutionary history of participants in multi-trophic interactions.
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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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