title: Herbivore exploits orally secreted bacteria to suppress plant defenses.
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.
authors.affiliation: 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.
authors.forename: Seung Ho
authors.initials: SH
authors.lastname: Chung
authors.forename: Cristina
authors.initials: C
authors.lastname: Rosa
authors.forename: Erin D
authors.initials: ED
authors.lastname: Scully
authors.forename: Michelle
authors.initials: M
authors.lastname: Peiffer
authors.forename: John F
authors.initials: JF
authors.lastname: Tooker
authors.forename: Kelli
authors.initials: K
authors.lastname: Hoover
authors.forename: Dawn S
authors.initials: DS
authors.lastname: Luthe
authors.forename: Gary W
authors.initials: GW
authors.lastname: Felton
mesh_terms: D000818:Animals; D000900:Anti-Bacterial Agents / Q000494:pharmacology; D001419:Bacteria / Q000187:drug effects / Q000276:immunology* / Q000648:ultrastructure; D004156:Catechol Oxidase / Q000378:metabolism; D001517:Coleoptera / Q000187:drug effects / Q000382:microbiology*; D003517:Cyclopentanes / Q000378:metabolism; D005408:Flagellin / Q000494:pharmacology; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D060434:Herbivory / Q000187:drug effects / Q000502:physiology*; D007814:Larva / Q000187:drug effects / Q000254:growth & development / Q000502:physiology; D018551:Solanum lycopersicum / Q000235:genetics / Q000276:immunology* / Q000382:microbiology*; D008969:Molecular Sequence Data; D009055:Mouth / Q000382:microbiology*; D054883:Oxylipins / Q000378:metabolism; D057865:Plant Immunity / Q000187:drug effects / Q000235:genetics; D018515:Plant Leaves / Q000382:microbiology / Q000648:ultrastructure; D020156:Salicylic Acid / Q000378:metabolism; D015398:Signal Transduction / Q000187:drug effects / Q000235:genetics; D013559:Symbiosis / Q000187:drug effects / Q000235:genetics
chemical_list: D000900:Anti-Bacterial Agents; D003517:Cyclopentanes; D054883:Oxylipins; D005408:Flagellin; C011006:jasmonic acid; D004156:Catechol Oxidase; D020156:Salicylic Acid
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