at a colloquium entitled " Self - Defense by Plants : Induction and Signalling Pathways , " organized

Genetic resistance in plants to root diseases is rare, and agriculture depends instead on practices such as crop rotation and soil fumigation to control these diseases. "Induced suppression" is a natural phenomenon whereby a soil due to microbiological changes converts from conducive to suppressive to a soilborne pathogen during prolonged monoculture of the susceptible host. Our studies have focused on the wheat root disease "take-all," caused by the fungus Gaeumannomyces graminis var. tritici, and the role of bacteria in the wheat rhizosphere (rhizobacteria) in a well-documented induced suppression (take-all decline) that occurs in response to the disease and continued monoculture of wheat. The results summarized herein show that antibiotic production plays a significant role in both plant defense by and ecological competence of rhizobacteria. Production of phenazine and phloroglucinol antibiotics, as examples, account for most of the natural defense provided by fluorescent Pseudomonas strains isolated from among the diversity of rhizobacteria associated with take-all decline. There appear to be at least three levels of regulation of genes for antibiotic biosynthesis: environmental sensing, global regulation that ties antibiotic production to cellular metabolism, and regulatory loci linked to genes for pathway enzymes. Plant defense by rhizobacteria producing antibiotics on roots and as cohabitants with pathogens in infected tissues is analogous to defense by the plant's production of phytoalexins, even to the extent that an enzyme of the same chalcone/stilbene synthase family used to produce phytoalexins is used to produce 2,4-diacetylphloroglucinol. The defense strategy favored by selection pressure imposed on plants by soilborne pathogens may well be the ability of plants to support and respond to rhizosphere microorganisms antagonistic to these pathogens. Growth and reproduction of the same plant species at the same sites year after year is the norm in natural plant communities. Crop rotation (alternate, pure-stand plantings of taxonomically very different plant species) is a novelty of agriculture used to manage soilborne pathogens and has no ecological equivalent in natural plant ecosystems. The continual presence of the same and related plant hosts in natural plant communities should favor pathogens below as well as above ground, yet curiously natural selection has produced abundant examples of useful genetic resistance to above-ground but not to below-ground pathogens. Selection pressure imposed by soilborne pathogens may favor a different defense strategynamely, plants with the ability, during monoculture, to support and respond to populations of rhizosphere microorganisms The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. antagonistic to their pathogens. The natural plant defense provided by microorganisms in the rhizosphere deserves much more scientific attention, both because of its importance in plant ecology and because of its potential as a practical means to improve the health and productivity of crop plants. We have focused on wheat rhizosphere bacteria (rhizobacteria) active against the pathogenic, soilborne fungus Gaeumannomyces graminis var. tritici, which is the cause of the root disease ofwheat known as "take-all." These beneficial bacteria are associated with a spontaneous take-all decline that occurs after two or three successive outbreaks of the disease with continuous cropping to wheat (1). Take-all decline is the most studied of several documented cases of "induced suppression" to a plant pathogen that develops in soil with monoculture of the susceptible host (2). The suppressiveness to take-all holds even when virulent inoculum of the pathogen is added to soil diluted by as much as 1:100 with disease-conducive soil (3). Studies of this suppression have pointed to a role of rhizobacteria of fluorescent Pseudomonas spp. inhibitory to the take-all pathogen (3-5). A population shift toward both higher numbers and a higher percentage of wheat rhizosphere-inhabiting fluorescent Pseudomonas spp. inhibitory in vitro to G. graminis var. tritici occurs as the soil undergoes conversion from conducive to suppressive to take-all (6). Yield increases of up to 33% have been obtained in performance trials using a seedtreatment method of application of fluorescent Pseudomonas spp. in fields infested with the take-all pathogen (refs. 7 and 8; R.J.C. and D.M.W., unpublished results). Some of the earliest studies on mechanisms of plant defense by rhizobacteria focused on the ability of the antagonist to produce siderophores with high affinity for iron, such as pyroverdin, thought to starve the pathogen for iron during its prepenetration and penetration activities in the rhizosphere (9-11). Competition for iron by rhizobacteria of fluorescent Pseudomonas spp. can potentiate competition for carbon by nonpathogenic fusaria interacting with the pathogen Fusarium oxysporum in the rhizosphere of plants in fusarium wiltsuppressive soils (12). In most cases, however, success in plant defense by these beneficial fluorescent pseudomonads also requires the ability to produce one or more antibiotics (13). Role of Antibiotics in Take-All Suppression Production of phenazine-1-carboxylate (PCA) accounts for 50-90% of take-all suppression by Pseudomonas fluorescens 2-79 (14), a strain obtained originally from the rhizosphere of Abbreviations: PCA, phenazine-1-carboxylate; Phz-, phenazinedeficient; Phl, 2,4-diacetylphloroglucinol; ORF, open reading frame; CHS/STS, chalcone synthase/stilbene synthase. *To whom reprint requests should be addressed.