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Plant Cell Advance Online Publication
Published on December 28, 2006; 10.1105/tpc.106.044180

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Received May 16, 2006
Returned for revision October 9, 2006
Accepted November 10, 2006

Phytotoxicity and Innate Immune Responses Induced by Nep1-Like Proteins

Dinah Qutob 1, Birgit Kemmerling 2, Frédéric Brunner 2, Isabell Küfner 2, Stefan Engelhardt 2, Andrea A. Gust 2, Borries Luberacki 2, Hanns Ulrich Seitz 2, Dietmar Stahl 3, Thomas Rauhut 4, Erich Glawischnig 4, Gabriele Schween 5, Benoit Lacombe 6, Naohide Watanabe 7, Eric Lam 7, Rita Schlichting 8, Dierk Scheel 8, Katja Nau 9, Gabriele Dodt 9, David Hubert 10, Mark Gijzen 1, and Thorsten Nürnberger 2*

1 Agriculture and Agri-Food Canada, London ON N5V 4T3, Canada
2 Center for Plant Molecular Biology-Plant Biochemistry, University of Tübingen, D-72076 Tübingen, Germany
3 PLANTA Angewandte Pflanzengenetik und Biotechnologie, D-37555 Einbeck, Germany
4 Department of Genetics, Technical University Munich, D-85350 Freising, Germany
5 Department of Plant Biotechnology, University of Freiburg, D-79104 Freiburg, Germany
6 Unité Mixte de Recherches Biochimie et Physiologie Moleculaire des Plantes, AgroM, Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Université Montpellier II, F-34060 Montpellier, France
7 Biotechnology Center for Agriculture and the Environment, Rutgers, The State University of New Jersey, New Brunswick, New Jersey 08901-8520
8 Department of Stress and Developmental Biology, Leibniz-Institute of Plant Biochemistry, D-06120 Halle/Saale, Germany
9 Department of Cellular Biochemistry, Interfaculty Institute of Biochemistry, University of Tübingen, D-72076 Tübingen, Germany
10 Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599

* To whom correspondence should be addressed. E-mail: nuernberger{at}uni-tuebingen.de.

We show that oomycete-derived Nep1 (for necrosis and ethylene-inducing peptide1)-like proteins (NLPs) trigger a comprehensive immune response in Arabidopsis thaliana, comprising posttranslational activation of mitogen-activated protein kinase activity, deposition of callose, production of nitric oxide, reactive oxygen intermediates, ethylene, and the phytoalexin camalexin, as well as cell death. Transcript profiling experiments revealed that NLPs trigger extensive reprogramming of the Arabidopsis transcriptome closely resembling that evoked by bacteria-derived flagellin. NLP-induced cell death is an active, light-dependent process requiring HSP90 but not caspase activity, salicylic acid, jasmonic acid, ethylene, or functional SGT1a/SGT1b. Studies on animal, yeast, moss, and plant cells revealed that sensitivity to NLPs is not a general characteristic of phospholipid bilayer systems but appears to be restricted to dicot plants. NLP-induced cell death does not require an intact plant cell wall, and ectopic expression of NLP in dicot plants resulted in cell death only when the protein was delivered to the apoplast. Our findings strongly suggest that NLP-induced necrosis requires interaction with a target site that is unique to the extracytoplasmic side of dicot plant plasma membranes. We propose that NLPs play dual roles in plant pathogen interactions as toxin-like virulence factors and as triggers of plant innate immune responses.




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