Herbivore exploits orally secreted bacteria to suppress plant defenses

Seung Ho Chung, Cristina Rosa, Erin D. Scully, Michelle Peiffer, John Frazier Tooker, Kelli Hoover, Dawn S. Luthe, Gary Felton

Research output: Contribution to journalArticle

176 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)15728-15733
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number39
DOIs
StatePublished - Sep 24 2013

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Herbivory
Salicylic Acid
Bacteria
Beetles
Larva
Lycopersicon esculentum
Pseudomonas
Insects
Stenotrophomonas
Anti-Bacterial Agents
Flagellin
Digestive System
Enterobacter
Aptitude
Solanum tuberosum
Gene Expression
jasmonic acid
Growth

All Science Journal Classification (ASJC) codes

  • General

Cite this

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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.",
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Herbivore exploits orally secreted bacteria to suppress plant defenses. / Chung, Seung Ho; Rosa, Cristina; Scully, Erin D.; Peiffer, Michelle; Tooker, John Frazier; Hoover, Kelli; Luthe, Dawn S.; Felton, Gary.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, No. 39, 24.09.2013, p. 15728-15733.

Research output: Contribution to journalArticle

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