David M. Weller
The Ruth Allen Award for research that has changed, or has the potential to change, the direction of research in any field of plant pathology is given this year to a team of three outstanding individuals for their work on the suppression of take-all disease of wheat. This work has served as a principal model system on which our current concepts of biological control of plant disease have been developed. Drs. R. James Cook, Linda Thomashow, and David Weller have worked together in the USDA-ARS Root Disease and Biological Control Research Laboratory on the Washington State University campus in Pullman, WA, to develop this system.
Because their individual efforts have been united in the study of a single system, they have developed a comprehensive view of the microbial interactions that govern disease development over time in agricultural fields. This view encompasses studies from the molecular to the community level, and each study has contributed in a meaningful way to the broad picture, rather than standing alone as an isolated fact.
Dr. Cook performed pioneering field experiments establishing that microorganisms were responsible for suppression of take-all disease of wheat, one of the most important diseases of wheat worldwide. His early studies in collaboration with Albert Rovira of CSIRO in South Australia attributed take-all decline, a phenomenon in which the severity of take-all declines with prolonged monoculture of wheat, to the presence of bacteria, particularly Pseudomonas spp., in take-all suppressive soil (i.e., those in which take-all has declined with monoculture). Subsequently, Drs. Cook and Weller demonstrated that fluorescent pseudomonads suppressive to the take-all fungus were present in greater numbers on roots of wheat grown in take-all suppressive soils than on roots grown in soils conducive to the disease. Strains of fluorescent pseudomonads isolated from the rhizosphere of wheat grown in suppressive soils were used as seed inoculants to mimic take-all decline.
The specific characteristics that contribute to suppression of take-all by the fluorescent pseudomonads were identified after Dr. Thomashow joined the Pullman team and initiated a genetic analysis of biological control traits exhibited by the disease-suppressive strains. Certain of the take-all suppressive strains, including Pseudomonas fluorescens 2-79, produced the antibiotic phenazine-l-carboxylic acid. From 2-79, Dr. Thomashow derived a series of transposon mutants that were deficient in phenazine production, cloned genes determining phenazine production, and complemented the mutants for phenazine production. When inoculated on wheat, mutants deficient in phenazine production were only 10-50% as effective as 2-79 or complemented mutants in suppressing take-all. A manuscript describing this study was the first published report demonstrating that an antibiotic contributed significantly to suppression of a soilborne fungal disease of plants. A later paper demonstrated the presence of phenazines in the rhizosphere of plants inoculated with a phenazine-producing strain of P. fluorescens, which provided the first definitive evidence for in situ production of an antifungal metabolite by bacteria inhabiting the root surface. More recently, the Pullman group demonstrated that isolates of the takeall fungus vary in their sensitivity to phenazine-l-carboxylic acid; this sensitivity correlates to their amenability to suppression by 2- 79 and other phenazine-producing strains of Pseudomonas spp. This correlation provides further evidence for the importance of antibiotic production in biological control of take-all by fluorescent pseudomonads and also points to variability in the pathogen population as an important source of variation in the success of biological control.