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PLANTS INTERACTING WITH OTHER ORGANISMS

Coordinated Regulation of Genes for Secretion in Tobacco at Late Developmental Stages: Association with Resistance against Oomycetes^1,[w]

Institut National de la Recherche Agronomique (INRA), Unité Interactions Plantes-Microorganismes, Villa Thuret, Boîte postale 2078, F–06606 Antibes cedex, France (K.H., M.-P.R., G.A., E.G.); Centre National de la Recherche Scientifique (CNRS), Institut de Pharmacologie Moléculaire et Cellulaire, 660 Route des Lucioles, 06560 Valbonne Sophia-Antipolis, France (C.M., M.A.D., P.B.); BASF Plant Science, Triangle Research Park, North Carolina, 27709 (J.C., C.W.); and Unité Mixte de Recherche Résponses des Organismes aux Stress Environnementaux, Génomique Fonctionnelle des Insectes, 1382, Route de Biot, 06560 Valbonne, France (K.H.)

Besides the systemic acquired resistance (SAR) induced in response to microbial stimulation, host plants may also acquire resistance to pathogens in response to endogenous stimuli associated with their own development. In tobacco (Nicotiana tabacum), the vegetative-to-flowering transition comes along with a susceptibility-to-resistance transition to the causal agent of black shank disease, the oomycete Phytophthora parasitica. This resistance affects infection effectiveness and hyphal expansion and is associated with extracellular accumulation of a cytotoxic activity that provokes in vitro cell death of P. parasitica zoospores. As a strategy to determine the extracellular events important for restriction of pathogen growth, we screened the tobacco genome for genes encoding secreted or membrane-bound proteins expressed in leaves of flowering plants. Using a signal sequence trap approach in yeast (Saccharomyces cerevisiae), 298 clones were selected that appear to encode for apoplastic, cell wall, or membrane-bound proteins involved in stress response, in plant defense, or in cell wall modifications. Microarray and northern-blot analyses revealed that, at late developmental stages, leaves were characterized by the coordinate up-regulation of genes involved in SAR and in peroxidative cross-linking of structural proteins to cell wall. This suggests the potential involvement of these genes in extracellular events that govern the expression of developmental resistance. The analysis of the influence of salicylic acid on mRNA accumulation also indicates a more complex network for regulation of gene expression at a later stage of tobacco development than during SAR. Further characterization of these genes will permit the formulation of hypotheses to explain resistance and to establish the connection with development.

¹ The CNRS/INRA Microarray facility was supported by grants from Groupement d'Intérêt Public Aventis, region Provence Alpes Côte d'Azur, CNRS, and INRA. This work was supported by INRA (fellowship to M.-P.R.) and by the Association pour la Recherche sur les Nicotianées (to M.-P.R.).

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

² These authors contributed equally to the paper.

³ Present address: Bayer CropScience, GenAvenir 1, 1 Rue Pierre Fontaine, 91 058 Evry cedex, France.

^* Corresponding author; e-mail galiana{at}antibes.inra.fr; fax 33–493–67–88–88.

Received October 1, 2003; returned for revision November 10, 2003; accepted November 10, 2003.

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