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PLANTS INTERACTING WITH OTHER ORGANISMS

Characterization of a Divinyl Ether Biosynthetic Pathway Specifically Associated with Pathogenesis in Tobacco^1,[W],[OA]

University of Turin, DiVaPRA-Plant Pathology, I–10095 Grugliasco. Turin, Italy (A.F., F.C.); Department of Plant Biochemistry, Albrech-von-Haller-Institute of Plant Sciences, Georg-August-University, D–37077 Goettingen, Germany (C.G., I.F.); and Université Paul Sabatier, Unité Mixte de Recherche, 5546 Centre National de la Recherche Scientifique-Université Paul Sabatier, Pôle de Biotechnologies Végétales, Auzeville F–31326 Castanet-Tolosan, France (L.M.-S., J.F., M.-T.E.-T.)

In tobacco (Nicotiana tabacum), an elicitor- and pathogen-induced 9-lipoxygenase (LOX) gene, NtLOX1, is essential for full resistance to pathogens, notably to an incompatible race of Phytophthora parasitica var. nicotianae (Ppn race 0). In this work, we aimed to identify those oxylipins induced during attempted infection by Ppn race 0 and down-regulated in NtLOX1 antisense plants. Here we show that colneleic and colnelenic acids, which significantly inhibit germination of Ppn zoospores, are produced in roots of wild-type plants inoculated with Ppn, but are down-regulated in NtLOX1 antisense plants. A search for a tobacco gene encoding the enzyme involved in the formation of these divinyl ether (DVE) fatty acids resulted in the cloning and characterization of a DVE synthase (DES) clone (NtDES1). NtDES1 is a 9-DES, specifically converting fatty acid 9-hydroperoxides into DVE fatty acids. NtDES1 has the potential to act in combination with NtLOX1 because, in the presence of the two enzymes, linoleic and linolenic acids were converted in vitro into colneleic and colnelenic acids, respectively. In addition, the pattern of NtDES1 gene expression was quite similar to that of NtLOX1. Their transcripts were undetected in healthy tissues from different plant organs, and accumulated locally and transiently after elicitation and fungal infection, but not after wounding. Visualization of NtDES1-yellow fluorescent protein and NtLOX1-cyan fluorescent protein fusion proteins in tobacco leaves indicated that both localize in the cytosol and are excluded from plastids, consistent with the presumed location of the 9-LOX pathway in plants and the lack of transit peptides for NtLOX1 and NtDES1, respectively. Our data suggest that, in tobacco, NtDES1 and NtLOX1 act together and form DVEs in response to pathogen attack and that this class of oxylipins modulates in vivo the outcome of the tobacco-Ppn race 0 interaction.

² These authors contributed equally to the paper.

³ Present address: Biochemistry and Molecular Biology Department, Michigan State University, 201 Biochemistry Building, East Lansing, MI 48824.

⁴ Present address: Laboratoire des Interactions Plantes Microorganismes, Unité Mixte de Recherche, Institut National de la Recherche Agronomique, Centre National de la Recherche Scientifique (441-2594), Chemin de Borde-Rouge, BP 52627, 31326 Castanet-Tolosan cedex, France.

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: Francesca Cardinale (francesca.cardinale{at}unito.it).

^[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.106.087304

^* Corresponding author; e-mail francesca.cardinale{at}unito.it; fax 39–011–236–8875.

Received July 25, 2006; accepted October 24, 2006; published November 3, 2006.

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