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PLANTS INTERACTING WITH OTHER ORGANISMS

Ethylene Modulates the Role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in Cross Talk between Salicylate and Jasmonate Signaling^1,[W],[OA]

Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, 3508 TB Utrecht, The Netherlands (A.L.-R., E.S.D.L., T.R., C.M.J.P.); Centre for BioSystems Genomics, 6700 AB Wageningen, The Netherlands (C.M.J.P.); Department of Biology, Duke University, Durham, North Carolina 27708–1000 (S.H.S.); Department of Biological Systems, RIKEN BioResource Center, Tsukuba 305–0074, Japan (H.A., M.K.); Department of Plant Pathology, National Agricultural Research Center, Tsukuba 305–8666, Japan (S.T.); and Plant Ecophysiology, Department of Biology, Faculty of Science, Utrecht University, 3508 TB Utrecht, The Netherlands (F.F.M., R.A.M.W.)

The plant hormones salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) play crucial roles in the signaling network that regulates induced defense responses against biotic stresses. Antagonism between SA and JA operates as a mechanism to fine-tune defenses that are activated in response to multiple attackers. In Arabidopsis (Arabidopsis thaliana), NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (NPR1) was demonstrated to be required for SA-mediated suppression of JA-dependent defenses. Because ET is known to enhance SA/NPR1-dependent defense responses, we investigated the role of ET in the SA-JA signal interaction. Pharmacological experiments with gaseous ET and the ET precursor 1-aminocyclopropane-1-carboxylic acid showed that ET potentiated SA/NPR1-dependent PATHOGENESIS-RELATED1 transcription, while it rendered the antagonistic effect of SA on methyl jasmonate-induced PDF1.2 and VSP2 expression NPR1 independent. This overriding effect of ET on NPR1 function in SA-JA cross talk was absent in the npr1-1/ein2-1 double mutant, demonstrating that it is mediated via ET signaling. Abiotic and biotic induction of the ET response similarly abolished the NPR1 dependency of the SA-JA signal interaction. Furthermore, JA-dependent resistance against biotic attackers was antagonized by SA in an NPR1-dependent fashion only when the plant-attacker combination did not result in the production of high levels of endogenous ET. Hence, the interaction between ET and NPR1 plays an important modulating role in the fine tuning of the defense signaling network that is activated upon pathogen and insect attack. Our results suggest a model in which ET modulates the NPR1 dependency of SA-JA antagonism, possibly to compensate for enhanced allocation of NPR1 to function in SA-dependent activation of PR genes.

² Present address: Institute of Molecular Plant Sciences, University of Edinburgh, Mayfield Road, Edinburgh EH9 3JR, United Kingdom.

³ Present address: Institute of Zoology, University of Neuchâtel, Emile-Argand 11, Neuchâtel, Switzerland.

⁴ Present address: De Ruiter Seeds, Leeuwenhoekweg 52, 2660 BB Bergschenhoek, The Netherlands.

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}uu.nl).

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

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.133926

^* Corresponding author; e-mail c.m.j.pieterse{at}uu.nl.

Received December 9, 2008; accepted January 25, 2009; published January 28, 2009.

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