Herbivore exploits orally secreted bacteria to suppress plant defenses.

Proceedings of the National Academy of Sciences of the United States of America (2013-09-11)
Seung Ho Chung, Cristina Rosa, Erin D Scully, Michelle Peiffer, John F Tooker, Kelli Hoover, Dawn S Luthe, Gary W Felton
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.

MATERIALS
Product Number
Brand
Product Description

Sigma-Aldrich
Salicylic acid, ACS reagent, ≥99.0%
Supelco
Salicylic acid, Pharmaceutical Secondary Standard; Certified Reference Material
Sigma-Aldrich
Salicylic acid, suitable for plant cell culture
Sigma-Aldrich
Salicylic acid, ≥99%, FG
Sigma-Aldrich
Salicylic acid, puriss. p.a., ≥99.0% (T)
Sigma-Aldrich
Salicylic acid, BioXtra, ≥99.0%
Sigma-Aldrich
Salicylic acid, meets analytical specification of Ph. Eur., BP, USP, 99.5-100.5% (calc. to the dried substance)
Sigma-Aldrich
Salicylic acid, ReagentPlus®, ≥99%
Supelco
Salicylic acid, certified reference material, TraceCERT®
Salicylic acid, European Pharmacopoeia (EP) Reference Standard
Supelco
Salicylic acid, 1.0 mg/mL in acetonitrile, ampule of 1 mL, certified reference material, Cerilliant®