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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Available from: Gary W Felton, Oct 05, 2015
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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.
    Ecological Entomology 10/2015; 40:620-628. DOI:10.1111/een.12235 · 1.70 Impact Factor
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    • "This study shows that FAW frass provides biochemical cues in the form of proteins that suppress herbivore defenses and increases herbivore performance on the plant. Since the frass protein extract used in our experiments was filtered through 0.2-μm filters, it is devoid of microorganisms, which previously have been found to play a role in influencing plant defenses (Chung et al. 2013). However, the effector-like molecule that mediates anti-herbivore defense suppression in caterpillar frass may be a protein of plant, caterpillar, or microbial origin that is present in the caterpillar gut. "
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    ABSTRACT: Caterpillar behaviors such as feeding, crawling, and oviposition are known to induce defenses in maize and other plant species. We examined plant defense responses to another important caterpillar behavior, their defecation. Fall armyworms (FAW, Spodoptera frugiperda), a major threat to maize (Zea mays), are voracious eaters and deposit copious amounts of frass in the enclosed whorl tissue surrounding their feeding site, where it remains for long periods of time. FAW frass is composed of molecules derived from the host plant, the insect itself, and associated microbes, and hence provides abundant cues that may alter plant defense responses. We observed that proteins from FAW frass initially induced wound-responsive defense genes in maize; however, a pathogenesis-related (pr) defense gene was induced as the time after application increased. Elicitation of pathogen defenses by frass proteins was correlated with increased herbivore performance and reduced fungal pathogen performance over time. These responses differ from the typical plant response to oral secretions of the FAW. The results pave the way for identification of protein molecule(s) from the excretion of an herbivore that elicits pathogen defense responses while attenuating herbivore defenses in plants.
    Journal of Chemical Ecology 08/2015; DOI:10.1007/s10886-015-0619-1 · 2.75 Impact Factor
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    • "Microbial-arthropod symbioses are ubiquitous interactions that are often critical to insect functioning, performance, and survival. Symbionts of insect herbivores have been shown to mediate interactions with natural enemies (Łukasik et al. 2013; Oliver et al. 2003; Scarborough et al. 2005), enable access to recalcitrant sources of carbon (Geib et al. 2008), contribute to nitrogen provisioning (Ayayee et al. 2014; Gündüz and Douglas 2009; Morales-Jiménez et al. 2013), circumvent plant defenses (Chung et al. 2013; North et al. 1997), and augment detoxification of allelochemicals (Boone et al. 2013; Dowd and Shen 1990; Hammerbacher et al. 2013; Kikuchi et al. 2012). Mechanisms of acquisition vary extensively . "
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    ABSTRACT: Microbial symbionts are becoming increasingly recognized as mediators of many aspects of plant - herbivore interactions. However, the influence of plant chemical defenses on gut associates of insect herbivores is less well understood. We used gypsy moth (Lymantria dispar L.), and differing trembling aspen (Populus tremuloides Michx.) genotypes that vary in chemical defenses, to assess the influence of foliar chemistry on bacterial communities of larval midguts. We evaluated the bacterial community composition of foliage, and of midguts of larvae feeding on those leaves, using next-generation high-throughput sequencing. Plant defense chemicals did not influence the composition of foliar communities. In contrast, both phenolic glycosides and condensed tannins affected the bacterial consortia of gypsy moth midguts. The two most abundant operational taxonomic units were classified as Ralstonia and Acinetobacter. The relative abundance of Ralstonia was higher in midguts than in foliage when phenolic glycoside concentrations were low, but lower in midguts when phenolic glycosides were high. In contrast, the relative abundance of Ralstonia was lower in midguts than in foliage when condensed tannin concentrations were low, but higher in midguts when condensed tannins were high. Acinetobacter showed a different relationship with host chemistry, being relatively more abundant in midguts than with foliage when condensed tannin concentrations were low, but lower in midguts when condensed tannins were high. Acinetobacter tended to have a greater relative abundance in midguts of insects feeding on genotypes with high phenolic glycoside concentrations. These results show that plant defense chemicals influence herbivore midgut communities, which may in turn influence host utilization.
    Journal of Chemical Ecology 12/2014; 41(1). DOI:10.1007/s10886-014-0530-1 · 2.75 Impact Factor
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