Coordinated Regulation of Genes for Secretion in Tobacco at Late Developmental Stages: Association with Resistance against Oomycetes  

Abstract

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.Establishment of acquired resistance to pathogens may be induced by physiological and/or developmental changes taking place in growing plants. The occurrence of a transition from susceptibility to resistance during development is a widely reported phenomenon in monocotyledons and dicotyledons in the case of viruses (Leisner et al., 1992(Leisner et al., , 1993, bacteria (Century et al., 1999;Kus et al., 2002), fungi (Moose and Sisco, 1994; Abedon and Tracy, 1996), and oomycetes (Reuveni et al., 1986;Wyatt et al., 1991: Hugot et al., 1999. Although this phenomenon, age-related resistance (ARR), is well documented from a pathological point of view, few studies have dealt with the genetic and molecular bases of disease control during plant development.On the contrary, numerous studies have investigated defense mechanisms activated in response to pathogen infection and associated with plant disease resistance (Hammond-Kosack and Parker, 2003). These studies have underlined the key role of the host extracellular space as sorting compartment of plant-pathogen interactions. At the early step of infection, the host plant recognizes some pathogensecreted molecules that elicit the coordinate activation of defense reactio...

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