The Nature and Application of Biocontrol Microbes III: Pseudomonas spp. Induced Systemic Resistance by Fluorescent Pseudomonas spp

Bakker, P. A. H. M., Pieterse, C. M. J., and van Loon, L. C. 2007. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239-243. Fluorescent Pseudomonas spp. have been studied for decades for their plant growth-promoting effects through effective suppression of soilborne plant diseases. The modes of action that play a role in disease suppression by these bacteria include siderophore-mediated competition for iron, antibiosis, production of lytic enzymes, and induced systemic resistance (ISR). The involvement of ISR is typically studied in systems in which the Pseudomonas bacteria and the pathogen are inoculated and remain spatially separated on the plant, e.g., the bacteria on the root and the pathogen on the leaf, or by use of split root systems. Since no direct interactions are possible between the two populations, suppression of disease development has to be plant-mediated. In this review, bacterial traits involved in Pseudomonas-mediated ISR will be discussed. Induced resistance is a state of enhanced defensive capacity developed by a plant reacting to specific biotic or chemical stimuli (42). In 1991, the research groups of B. Schippers in Baarn, The Netherlands, and J. W. Kloepper in Auburn, AL, discovered independently that induced systemic resistance (ISR) is a mode of action of plant growth-promoting rhizobacteria (PGPR), especially fluorescent pseudomonads, in suppressing diseases (43,49). The Pseudomonas bacteria were inoculated into the rhizosphere and remained spatially separated from the pathogen that was inoculated on the aboveground plant parts, either into the stem (43) or on the leaf surface (49). By ensuring spatial separation between the Pseudomonas bacteria and the pathogen on the root system, for instance in a split root system, it was demonstrated that ISR is also effective against root-infecting pathogens (15,52). A threshold population density of 10 colony forming units per gram of root was required for effectiveness of the resistance-inducing Pseudomonas strain (32). When used under commercial greenhouse conditions, the ISR triggering P. fluorescens strain WCS374r significantly protected radish from Fusarium wilt leading to average yield increases of 40% (17). In the last decade it has become clear that elicitation of ISR is a widespread phenomenon, not only for fluorescent pseudomonads but for a variety of nonpathogenic microorganisms and biological control agents. ISR is phenotypically similar to systemic acquired resistance (SAR) that is triggered by necrotizing pathogens in that disease caused by a challenging pathogen is reduced. Accumulation of salicylic acid (SA) in the plant is required for SAR (40). In transgenic plants that constitutively express the nahG gene, a salicylate hydroxylase gene from P. putida, SA cannot accumulate and, accordingly, these plants no longer express SAR (8). The SA-dependent SAR pathway can also be triggered by applying SA exogenously. In Arabidopsis thaliana, ISR by P. fluorescens WCS417r is independent of SA accumulation as it is still operative in NahG plants (28). From experiments with mutants of Arabidopsis that are nonor less responsive to ethylene or jasmonic acid (JA), it was concluded that an intact response to these plant hormones is required for expression of ISR, whereas SAR is still expressed in these mutants (29). Both ISR and SAR are effective against a wide range of pathogens. However, there are differences in the effectiveness of the signaling compounds involved against different types of pathogens. In Arabidopsis, SAR is effective against pathogens that in noninduced plants are resisted through SA-dependent defenses, whereas ISR is effective against pathogens that are resisted through JA/ethylene-dependent defenses (41). This suggested that the range of pathogens that are controlled might be extended when ISR and SAR are combined. Interestingly, when ISR and SAR are activated simultaneously, enhanced disease suppression occurs against pathogens against which both SA and JA/ethylene responses are effective, such as P. syringae pv. tomato (45). Thus, there appears to be room to increase the effectiveness of induced resistance. To manipulate this phenomenon effectively for practical applications, knowledge on bacterial traits involved in the triggering of ISR is essential. In this paper, we will focus on the determinants of Pseudomonas that are involved in triggering ISR (an overview of the determinants is presented in Table 1) and discuss future directions of research. Flagella. Bacterial flagellins, the main protein component of flagella, can elicit defense responses in plants (9,53). For P. putida strain WCS358, the involvement of flagella in ISR was studied in Arabidopsis, bean, and tomato by applying isolated flagella and by using nonmotile mutants that lack flagella (23). In Arabidopsis, application of WCS358 flagella triggered ISR against P. syringae pv. tomato, whereas in bean or tomato, their application did not lead to induced resistance. Moreover, a mutant of WCS358 that lacks flagella was as effective in triggering ISR in Arabidopsis as the parental strain, and it was concluded that there are additional determinants in strain WCS358 that can induce resistance. These results suggest that although flagella can be involved in ISR, they are not the main trigger for this Pseudomonas strain. Lipopolysaccharides. Reports that cell surface components of pathogenic bacteria can induce resistance (10,24) stimulated a study on the possible involvement of lipopolysaccharides (LPS) Corresponding author: P. A. H. M. Bakker E-mail address: [email protected] DOI: 10.1094 / PHYTO-97-2-0239 © 2007 The American Phytopathological Society