Syringolin Reprograms Wheat to Undergo Hypersensitive Cell Death in a Compatible Interaction with Powdery Mildew

Abstract

We had previously isolated and characterized syringolin A, one of the molecular determinants secreted by Pseudomonas syringae pv syringae that is perceived by nonhost plant species such as rice. Here, we show that syringolin A is recognized by wheat and that it induces the accumulation of gene transcripts and increases protection against powdery mildew when applied before inoculation. Moreover, syringolin A essentially eradicates powdery mildew from infected wheat if applied after inoculation. This curative effect is accompanied by the induction of cell death and the reactivation of pathogenesis-related genes whose transcript levels initially accumulate after powdery mildew inoculation but then decline during the later course of infection. Because syringolin A has no fungicidal activity against a variety of fungi and its action on wheat cannot be mimicked by the fungicide cyprodinil, syringolin A is hypothesized to counteract the suppression of host defense reactions imposed by the pathogen on the colonized cells. INTRODUCTIONPlants have evolved a variety of passive and active defense mechanisms against a plethora of potentially pathogenic microbes. A prominent form of an active defense response is the hypersensitive reaction, which is accompanied by localized cell death at the infection site and results in complete resistance. It has been demonstrated in many systems that these local events can induce systemic acquired resistance, that is, they cause the establishment of a physiological state in a plant that makes the plant more resistant to a variety of pathogens to which it normally would be susceptible (Hunt and Ryals, 1996;Sticher et al., 1997). A prerequisite for active defense reactions to occur is recognition of the attacking microbe by the plant. In a number of systems exhibiting race-specific resistance according to the gene-forgene concept, genes governing the recognition process have been molecularly characterized (Hammond-Kosack and Jones, 1996; Baker et al., 1997;Ellis and Jones, 1998;Nürnberger, 1999). Phenotypically, active defense reactions evoked by nonhost pathogens are very similar to the ones observed in race-specific incompatible interactions. However, the molecular events underlying the recognition process between plants and nonhost pathogens have been less well characterized, mainly because genetic analysis was hampered by the apparent redundancy built into the system.In rice, acquired resistance against the rice blast fungus Magnaporthe grisea can be induced by inoculation with the nonhost pathogen Pseudomonas syringae pv syringae (Smith and Métraux, 1991). We have recently isolated syringolin A, one of the bacterial determinants that are recognized by rice plants and cultured rice cells (Wäspi et al., 1998a;Hassa et al., 2000). Syringolin A (Figure 1) belongs to a family of small, structurally closely related peptides (syringolin A to F) that are synthesized nonribosomally and secreted by P. s. syringae (Wäspi et al., 1998a(Wäspi et al., , 1999. Application of isolated syringolin A in m...

Nitric Oxide and ProteinS-Nitrosylation Are Integral to Hydrogen Peroxide-Induced Leaf Cell Death in Rice

“…Dead cells were stained using detached leaves by a method modified previously (Wäspi et al, 2001). Leaves of 2-month-old wild-type and noe1 plants were submerged in trypan blue solution at 70°C for 10 min and then heated in boiling water for 2 min and left staining overnight.…”

Peroxisomal Hydrogen Peroxide Is Coupled to Biotic Defense Responses by ISOCHORISMATE SYNTHASE1 in a Daylength-Related Manner

“…Dead cells were stained in detached rosette leaves as described ) using a method modified from Wäspi et al (2001). Percentage lesion areas were quantified using IQmaterials software.…”

Alpha-picolinic acid, a fungal toxin and mammal apoptosis-inducing agent, elicits hypersensitive-like response and enhances disease resistance in rice

“…For instance, syringolin A isolated from the nonhost pathogen Pseudomonas syringae pv syringae initiated wheat hypersensitive cell death and enhanced resistance to powdery mildew, and was also recognized by rice cell [19]. The fungal cerebrosides including cerebrosides B1 and C were shown to elicit the hypersensitive cell death and phytoalexin accumulation in rice plants [20].…”