Seung Ho Chunga, Cristina Rosaa, Erin D. Scullyb, Michelle Peiffera, John F. Tookera, Kelli Hoovera, Dawn S. Luthec, and Gary W. Feltona,1
Departments of aEntomology and
cPlant Science, Center for Chemical Ecology, and
bIntercollege Program in Genetics, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA 16802
Edited by James H. Tumlinson, Pennsylvania State University, University Park, PA, and approved July 11, 2013 (received for review May 15, 2013)
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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Author contributions: S.H.C., C.R., E.D.S., K.H., and G.W.F. designed research; S.H.C. and M.P. performed research; J.F.T. and D.S.L. contributed new reagents/analytic tools; S.H.C. and G.W.F. analyzed data; and S.H.C., C.R., E.D.S., J.F.T., K.H., D.S.L., and G.W.F. wrote the paper.