First published online July 7, 2006; 10.1104/pp.106.083907
Plant Physiology 142:352-363 (2006)
© 2006 American Society of Plant Biologists
PLANTS INTERACTING WITH OTHER ORGANISMS
Herbivore-Induced Resistance against Microbial Pathogens in Arabidopsis1
Martin De Vos2,
Wendy Van Zaanen,
Annemart Koornneef,
Jerôme P. Korzelius,
Marcel Dicke,
L.C. Van Loon and
Corné M.J. Pieterse*
Graduate School of Experimental Plant Sciences, Section of Phytopathology, Institute of Environmental Biology, Utrecht University, 3508 TB Utrecht, The Netherlands (M.D.V., W.V.Z., A.K., J.P.K., L.C.V.L., C.M.J.P.); and Graduate School of Experimental Plant Sciences, Laboratory of Entomology, Wageningen University, 6700 EH Wageningen, The Netherlands (M.D.)
Caterpillars of the herbivore Pieris rapae stimulate the production of jasmonic acid (JA) and ethylene (ET) in Arabidopsis (Arabidopsis thaliana) and trigger a defense response that affects insect performance on systemic tissues. To investigate the spectrum of effectiveness of P. rapae-induced resistance, we examined the level of resistance against different pathogens. Although the necrotrophic fungus Alternaria brassicicola is sensitive to JA-dependent defenses, herbivore-induced resistance was not effective against this pathogen. By contrast, caterpillar feeding significantly reduced disease caused by the bacterial pathogens Pseudomonas syringae pv tomato and Xanthomonas campestris pv armoraciae. However, this effect was apparent only locally in caterpillar-damaged tissue. Arabidopsis mutants jar1, coi1, ein2, sid2, eds5, and npr1 showed wild-type levels of P. rapae-induced protection against P. syringae pv tomato, suggesting that this local, herbivore-induced defense response does not depend exclusively on either JA, ET, or salicylic acid (SA). Resistance against the biotroph Turnip crinkle virus (TCV) requires SA, but not JA and ET. Nevertheless, herbivore feeding strongly affected TCV multiplication and TCV lesion formation, also in systemic tissues. Wounding alone was not effective, but application of P. rapae regurgitate onto the wounds induced a similar level of protection. Analysis of SA-induced PATHOGENESIS RELATED-1 (PR-1) expression revealed that P. rapae grazing primed Arabidopsis leaves for augmented expression of SA-dependent defenses. Pharmacological experiments showed that ET acts synergistically on SA-induced PR-1, suggesting that the increased production of ET upon herbivore feeding sensitizes the tissue to respond faster to SA, thereby contributing to an enhanced defensive capacity toward pathogens, such as TCV, that trigger SA-dependent defenses upon infection.
1 This work was supported in part by the Earth and Life Sciences Foundation (grant nos. 865–04–002 and 813–06–002), which is subsidized by the Netherlands Organization of Scientific Research.
2 Present address: Boyce Thompson Institute for Plant Research, Tower Rd., Cornell Campus, Ithaca, NY 15853.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Corné M.J. Pieterse (c.m.j.pieterse{at}bio.uu.nl).
www.plantphysiol.org/cgi/doi/10.1104/pp.106.083907
* Corresponding author; e-mail c.m.j.pieterse{at}bio.uu.nl; fax 31–30–2518366.
Received May 22, 2006;
accepted June 26, 2006.
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