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Published on May 20, 2009; 10.1104/pp.109.139550

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Received April 11, 2009
Accepted May 14, 2009

Different Lepidopteran Elicitors Account for Crosstalk in Herbivory-induced Phytohormone Signaling

Celia Diezel , Caroline von Dahl , Emmanuel Gaquerel , and Ian T. Baldwin *

Department of Molecular Ecology, Max-Planck-Institute for Chemical Ecology, Beutenberg Campus, Hans-Knoll Strasse 8, D-07745 Jena, Germany

* Corresponding author; email: Baldwin{at}ice.mpg.de.

Salicylic acid (SA), jasmonic acid (JA), ethylene (ET) and their interactions mediate plant responses to pathogen and herbivore attack. JA/SA and JA/ET cross-signaling are well studied but little is known about SA/ET cross-signaling in plant-herbivore interactions. When the specialist herbivore Manduca sexta attacks Nicotiana attenuata rapid and transient JA and ET bursts are elicited without significantly altering wound-induced SA levels. In contrast, attack from the generalist Spodoptera exigua results in comparatively lower JA and ET bursts, but amplified SA bursts. These phytohormone responses are mimicked when the species' larval oral secretions (OSSe and OSMs) are added to puncture wounds. Fatty acid- amino acid conjugates (FACs) elicit the JA and ET bursts, but not the SA burst. OSSe had enhanced glucose oxidase (GOX) activity (but not {beta}-glucosidase activity) which was sufficient to elicit the SA burst and attenuate the JA and ET levels. It is known that SA antagonizes JA; GOX activity and associated H2O2 also antagonizes the ET burst. We examined the OSMs-elicited SA burst in plants impaired in their ability to elicit JA(as-lox3) and ET(ir-aco) bursts and perceive ET(35s-etr1b) after FAC elicitation, which revealed that both ET and JA bursts antagonize the SA burst. Treating WT plants with ethephone and 1-methylcyclopropane confirmed these results and demonstrated the central role of the ET burst in suppressing the OSMs-elicited SA burst. By suppressing the SA burst, the ET burst likely facilitates unfettered JA-mediated defense activation in response to herbivores which otherwise would elicit SA.






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