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PLANTS INTERACTING WITH OTHER ORGANISMS

Differential Timing of Spider Mite-Induced Direct and Indirect Defenses in Tomato Plants^1,[w]

Institute for Biodiversity and Ecosystem Dynamics (M.R.K., M.W.S.) and Swammerdam Institute for Life Sciences, Department of Plant Physiology, University of Amsterdam, 1098 SM Amsterdam, The Netherlands (K.A., M.A.H., R.C.S.)

Through a combined metabolomics and transcriptomics approach we analyzed the events that took place during the first 5 d of infesting intact tomato (Lycopersicon esculentum) plants with spider mites (Tetranychus urticae). Although the spider mites had caused little visible damage to the leaves after 1 d, they had already induced direct defense responses. For example, proteinase inhibitor activity had doubled and the transcription of genes involved in jasmonate-, salicylate-, and ethylene-regulated defenses had been activated. On day four, proteinase inhibitor activity and particularly transcript levels of salicylate-regulated genes were still maintained. In addition, genes involved in phospholipid metabolism were up-regulated on day one and those in the secondary metabolism on day four. Although transcriptional up-regulation of the enzymes involved in the biosynthesis of monoterpenes and diterpenes already occurred on day one, a significant increase in the emission of volatile terpenoids was delayed until day four. This increase in volatile production coincided with the increased olfactory preference of predatory mites (Phytoseiulus persimilis) for infested plants. Our results indicate that tomato activates its indirect defenses (volatile production) to complement the direct defense response against spider mites.

² These authors contributed equally to the paper.

^[w] The online version of this article contains Web-only data.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.038315.

^* Corresponding author; e-mail kant{at}science.uva.nl; fax 31–20–5257754.

Received December 22, 2003; returned for revision February 12, 2004; accepted February 17, 2004.

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