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Interactions Between Plants and Beneficial Pseudomonas Spp Antonie van Leeuwenhoek (2007) 92:367–389 DOI 10.1007/s10482-007-9167-1 REVIEW PAPER Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection Jesu´s Mercado-Blanco Æ Peter A. H. M. Bakker Received: 9 January 2007 / Accepted: 12 March 2007 / Published online: 21 June 2007 Ó Springer Science+Business Media B.V. 2007 Abstract Specific strains of fluorescent Pseudomo- Abbreviations nas spp. inhabit the environment surrounding plant AHL N-acyl-homoserine lactone roots and some even the root interior. Introducing DAPG 2,4-diacetylphloroglucinol such bacterial strains to plant roots can lead to ISR Induced systemic resistance increased plant growth, usually due to suppression of PCA Phenazine-1-carboxylic acid plant pathogenic microorganisms. We review the PGPR Plant growth promoting rhizobacteria modes of action and traits of these beneficial SA Salicylic acid Pseudomonas bacteria involved in disease suppres- SAR Systemic acquired resistance sion. The complex regulation of biological control TAD Take-all decline traits in relation to the functioning in the root environment is discussed. Understanding the com- plexity of the interactions is instrumental in the exploitation of beneficial Pseudomonas spp. in con- Introduction trolling plant diseases. Plant–bacteria interactions are long known and have Keywords Antibiotics Á Biocontrol Á Endophytes Á three well-differentiated manifestations. The first is a Induced resistance Á Plant-growth promotion Á direct relation between plants and pathogenic bacteria Siderophores (for instance, Agrobacterium spp., Erwinia spp., Ralstonia spp., etc.), causing a state of disease. In this case the consequences for the plant are negative. A second type is a direct interaction between plants and non-pathogenic bacteria (for example, Azorhizo- J. Mercado-Blanco (&) bium, Bradyrhizobium, Rhizobium, Sinorhizobium, Departamento de Proteccio´n de Cultivos, Instituto de etc.), leading to a beneficial association for both Agricultura Sostenible, Consejo Superior de partners. This interaction is a mutualistic symbiosis, Investigaciones Cientı´ficas (CSIC), Apartado 4084, 14080 Cordoba, Spain yielding positive effects for the plant. These two e-mail: [email protected] types of interactions arise as a consequence of fine- tuned molecular signalling between the bacteria and P. A. H. M. Bakker the plants. However, the ultimate boundaries between Plant Microbe Interactions, Institute of Environmental Biology, Utrecht University, P.O. Box a mutualistic and a pathogenic interaction can be 80084, 3508 TB Utrecht, The Netherlands fuzzy, and the recognition and signal-transduction 123 368 Antonie van Leeuwenhoek (2007) 92:367–389 processes leading to the plant response may be et al. 2006). Some of these beneficial bacteria do similar for both types of interactions (Baron and induce plant responses other than growth promotion. Zambryski 1995; Soto et al. 2006). Thus, studies on For example, they can promote a state of enhanced the Sinorhizobium meliloti-alfalfa mutualistic symbi- defensive capacity against pathogen attack (Sticher osis have independently shown: (i) induction by et al. 1997; van Loon et al. 1998). Protection against bacteria of a hypersensitive response (HR) in com- plant pathogens can also be a consequence of direct patible interactions that could be part of a plant antagonistic interactions between beneficial bacteria mechanism to control the number of successful and pathogens. In this case, the rhizosphere is just the infections (Vasse et al. 1993); (ii) prevention of host ecological niche where beneficial bacteria and delete- defence response by rhizobia (McKhann et al. 1997); rious microorganisms live, feed and encounter. Even- or (iii) accumulation of salicylic acid (SA) and H2O2 tually, the plant becomes the battle-field where the in roots inoculated with either NodÀ (nodulation) beneficial and deleterious organisms compete for mutants or incompatible rhizobia in contrast with the resources. Obviously the consequences can be of inoculation with compatible strains, suggesting an extreme importance for the plant, and it is likely that involvement of the Nod factors in the inhibition of the plant somehow influences the development and SA-mediated defence response in legumes (Martı´nez- results of these microbial interactions. Abarca et al. 1998; Bueno et al. 2001). These findings This review will focus on the interaction of plant show a resemblance between mutualistic Rhizobia- roots with beneficial Pseudomonas spp., a group of legume and pathogenic bacteria–plant interactions. bacteria that has been studied for direct plant-growth The third type of interaction that numerous bacterial promotion as well as their abilities to control plant genera (e.g. Alcaligenes spp., Bacillus spp., Pseudo- diseases (O’Sullivan and O’Gara 1992). Both aspects monas spp., Serratia spp., etc.) establish with plants confer this bacterial group as an alternative for in principle could be considered as neutral for the replacing (or reducing) the use of agrochemicals, plant. Strictly speaking, they do not fit to the which fits environmentally-friendly strategies to be definition of pathogenic or mutualistic bacteria, implemented in a modern sustainable agriculture because of the absence of the evident negative or framework. Understanding the interactions between positive effects. However, there has been an increas- the plant, beneficial pseudomonads, and plant patho- ing body of literature that describes these bacteria as gens are of crucial importance to overcome practical clearly beneficial to plants, either because they problems such as the inconsistency of biocontrol directly promote plant growth (Glick 1995; Bashan performance. and Holguin 1998) or they protect plants against a broad range of phytopathogens and pests (Kerry 2000; Ramamoorthy et al. 2001; Gerhardson 2002). Beneficial (non-deleterious) Pseudomonas spp. Direct plant growth-promoting effects of bacteria that specified inhabit the rhizosphere have been attributed to provision of nutrients, microelements, hormones, Pseudomonas spp. form a diverse group of aerobic, etc., to the plant. These bacteria seem therefore to Gram-negative, chemoheterotrophic, motile, rod- exert their positive effects by a non-active way, shaped bacteria. Of particular interest to this review colonizing the surface of plant tissues and providing is the subset of RNA group I (Palleroni et al. 1973) profitable compounds to the plant. Some of these species characterized by the distinctive production bacteria go a step further and intimately establish of yellow-green fluorescent pigments with sidero- within plant tissues as endophytes (Rosenblueth and phore activity (pyoverdins or pseudobactins) (see Martı´nez-Romero 2006), without causing any evident below). They are very versatile bacteria, found damage or morphological changes in the plant. abundantly and ubiquitously in nature, and well- Whether this endophytic establishment is the conse- adapted to numerous ecological niches due to rather quence of an active interaction between plant and simple nutritional requirements. Members of this bacterium is poorly investigated, although the genome group are important as human, animal and plant sequencing of some of them, as Azoarcus sp., will be pathogens and in food spoilage. The genomes of instrumental in explaining their behaviour (Krause several Pseudomonas spp. are available (Stover 123 Antonie van Leeuwenhoek (2007) 92:367–389 369 et al. 2000; Nelson et al. 2002; Paulsen et al. complex, continuous and delicate balance among a 2005), revealing genome sizes larger (>5,500 large array of biotic (the plant, the beneficial ORFs) than most other sequenced bacterial colonizer, other microorganisms, etc.) and abiotic genomes, although similar or even smaller than (soil type, water and mineral contents, pH, temper- genome sizes of other plant-associated bacteria (i.e. ature, composition of root exudates, nutrient avail- Agrobacterium tumefaciens, Sinorhizobium meliloti ability, etc.) factors (Loper et al. 1985; Acea and or Mesorhizobium loti) (Van Sluys et al. 2002). Alexander 1988; Bahme and Schroth 1987; Howie Pseudomonads interacting with plants include phy- et al. 1987; Kwok et al. 1987; Stephens et al. 1987; topathogens grouped in the species Pseudomonas Lam 1990). To determine the contributions of these syringae. This species is subdivided into pathovars factors as well as their interactions is of crucial on the basis of host specificity, and they are the importance, and gaps in this knowledge may aetiological agents of leaf spots, blights, and wilts explain why practical application of PGPR suffers in susceptible host plants (Gardan et al. 1991, from inconsistent performance (Thomashow 1996). 1999; Young and Triggs 1994). Other members (for In the hostile and nutrient-limiting bulk soil example, certain P. fluorescens P. putida,or environment, plant roots and their immediate P. aeruginosa strains) are known to be beneficial vicinity are extremely attractive places for both to plants. Some strains have been recognized for a beneficial and deleterious soil borne microbes. The long time as biocontrol agents (Howell and Stipa- roots and the rhizosphere offer an ecological niche novic 1980; Lifshitz et al. 1986; Xu and Gross that provides an important source of a wide range 1986; Weller 1988). They are also known as plant of nutrients (Degenhardt et al. 2003). The estab- growth promoting rhizobacteria (PGPR), either lishment of the microbe–plant interaction is pre- per
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