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.

Download full-text


Available from: Gary W Felton,
101 Reads
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    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
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Above- and belowground plant parts are simultaneously attacked by different pests and pathogens. The host mediates these interactions and physiologically reacts, e.g. with local and systemic alterations of endogenous hormone levels coupled with coordinated transcriptional changes. This in turn affects attractiveness and susceptibility of the plant to subsequent attackers. Here, the model plant Arabidopsis thaliana is used to study stress hormone-based systemic responses triggered by simultaneous root parasitism by the cyst nematode Heterodera schachtii and shoot herbivory by the thrips Frankliniella occidentalis and the spider mite Tetranychus urticae. First, HPLC/MS and quantitative reverse transcriptase PCR are used to show that nematode parasitism strongly affects stress hormone levels and expression of hormone marker genes in shoots. Previous nematode infection is then demonstrated to affect the behavioural and life history performance of both arthropods. While thrips explicitly avoid nematode-infected plants, spider mites prefer them. In addition, the life history performance of T. urticae is significantly enhanced by nematode infection. Finally, systemic changes triggered by shoot-feeding F. occidentalis but not T. urticae are shown to make the roots more attractive for H. schachtii. This work emphasises the importance of above- and belowground signalling and contributes to a better understanding of plant systemic defence mechanisms against plant-parasitic nematodes. © The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology.
    Journal of Experimental Botany 08/2015; DOI:10.1093/jxb/erv398 · 5.53 Impact Factor
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    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; 41(9). DOI:10.1007/s10886-015-0619-1 · 2.75 Impact Factor
Show more