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Comparative genomics of plant-asssociated Pseudomonas spp.: Insights into diversity and inheritance of traits involved in multitrophic interactions
Loper, J.E. ; Hassan, K.A. ; Mavrodi, D.V. ; Davis II, E.W. ; Lim, C.K. ; Shaffer, B.T. ; Elbourne, L.D.H. ; Stockwell, V.O. ; Hartney, S.L. ; Breakwell, K. ; Henkels, M.D. ; Tetu, S.G. ; Rangel, L.I. ; Kidarsa, T.A. ; Wilson, N.L. ; Mortel, J.E. van de; Song, C. ; Blumhagen, R. ; Radune, D. ; Hostetler, J.B. ; Brinkac, L.M. ; Durkin, A.C. ; Kluepfel, D.A. ; Wechter, W.P. ; Anderson, A.J. ; Kim, Y.C. ; Pierson III, L.S. ; Pierson, E.A. ; Lindow, S.E. ; Kobayashi, D.Y. ; Raaijmakers, J. ; Weller, D.M. ; Thomashow, L.S. ; Allen, A.E. ; Paulsen, I.T. - \ 2012
Plos Genetics 8 (2012)7. - ISSN 1553-7404
iii secretion system - syringae pv. syringae - gamma-aminobutyric-acid - biological-control - fluorescens pf-5 - biocontrol strain - antibiotic production - secondary metabolite - phenylacetic acid - chlororaphis o6
We provide here a comparative genome analysis of ten strains within the Pseudomonas fluorescens group including seven new genomic sequences. These strains exhibit a diverse spectrum of traits involved in biological control and other multitrophic interactions with plants, microbes, and insects. Multilocus sequence analysis placed the strains in three sub-clades, which was reinforced by high levels of synteny, size of core genomes, and relatedness of orthologous genes between strains within a sub-clade. The heterogeneity of the P. fluorescens group was reflected in the large size of its pan-genome, which makes up approximately 54% of the pan-genome of the genus as a whole, and a core genome representing only 45–52% of the genome of any individual strain. We discovered genes for traits that were not known previously in the strains, including genes for the biosynthesis of the siderophores achromobactin and pseudomonine and the antibiotic 2-hexyl-5-propyl-alkylresorcinol; novel bacteriocins; type II, III, and VI secretion systems; and insect toxins. Certain gene clusters, such as those for two type III secretion systems, are present only in specific sub-clades, suggesting vertical inheritance. Almost all of the genes associated with multitrophic interactions map to genomic regions present in only a subset of the strains or unique to a specific strain. To explore the evolutionary origin of these genes, we mapped their distributions relative to the locations of mobile genetic elements and repetitive extragenic palindromic (REP) elements in each genome. The mobile genetic elements and many strain-specific genes fall into regions devoid of REP elements (i.e., REP deserts) and regions displaying atypical tri-nucleotide composition, possibly indicating relatively recent acquisition of these loci. Collectively, the results of this study highlight the enormous heterogeneity of the P. fluorescens group and the importance of the variable genome in tailoring individual strains to their specific lifestyles and functional repertoire
Diversity and Evolution of the Phenazine Biosynthesis Pathway
Mavrodi, D.V. ; Peever, T.L. ; Mavrodi, O.V. ; Parejko, J.A. ; Raaijmakers, J.M. ; Lemanceau, P. ; Mazurier, S. ; Heide, L. ; Blankenfeldt, W. ; Weller, D.M. ; Thomashow, L.S. - \ 2010
Applied and Environmental Microbiology 76 (2010)3. - ISSN 0099-2240 - p. 866 - 879.
burkholderia-cepacia complex - pseudomonas-chlororaphis pcl1391 - erwinia-herbicola eh1087 - phenazine-1-carboxylic acid - fluorescent pseudomonas - biological-control - virulence factors - genome sequence - aeruginosa pao1 - gene-cluster
Phenazines are versatile secondary metabolites of bacterial origin that function in biological control of plant pathogens and contribute to the ecological fitness and pathogenicity of the producing strains. In this study, we employed a collection of 94 strains of various geographic, environmental and clinical origins to study the distribution and evolution of phenazine genes in members of Pseudomonas, Burkholderia, Pectobacterium, Brevibacterium and Streptomyces genera. Our results confirmed the diversity of phenazine producers and revealed that most of them appear to be soil-dwelling and/or plant-associated species. Genome analyses and comparisons of phylogenies inferred from sequences of the key phenazine biosynthesis phzF and housekeeping genes (rrs, recA, rpoB, atpD, and gyrB) revealed that the evolution and dispersal of phenazine genes is driven by mechanisms ranging from conservation in Pseudomonas spp. to horizontal gene transfer in Burkholderia spp. and Pectobacterium spp. DNA extracted from cereal crop rhizospheres and screened for the presence of phzF contained sequences consistent with a diverse population of phenazine-producers in commercial farm fields located in central Washington State, thus providing the first evidence of U.S. soils enriched in indigenous phenazine-producing bacteria
Microbial populations responsible for specific soil suppressiveness to plant pathogens
Weller, D.M. ; Raaijmakers, J.M. ; McSpadden Gardener, B.B. ; Thomashow, L.S. - \ 2002
Annual Review of Phytopathology 40 (2002). - ISSN 0066-4286 - p. 309 - 348.
Agricultural soils suppressive to soilborne plant pathogens occur worldwide, and for several of these soils the biological basis of suppressiveness has been described. Two classical types of suppressiveness are known. General suppression owes its activity to the total microbial biomass in soil and is not transferable between soils. Specific suppression owes its activity to the effects of individual or select groups of microorganisms and is transferable. The microbial basis of specific suppression to four diseases, Fusarium wilts, potato scab, apple replant disease, and take-all, is discussed. One of the best-described examples occurs in take-all decline soils. In Washington State, take-all decline results from the buildup of fluorescent Pseudomonas spp. that produce the antifungal metabolite 2,4-diacetylphloroglucinol. Producers of this metabolite may have a broader role in disease-suppressive soils worldwide. By coupling molecular technologies with traditional approaches used in plant pathology and microbiology, it is possible to dissect the microbial composition and complex interactions in suppressive soils.
Differential ability of genotypes of 2,4-Diacetylphloroglucinol-producing Pseudomonas fluorescens strains to colonize the roots of pea plants
Landa, B.B. ; Mavrodi, O.V. ; Raaijmakers, J.M. ; McSpadden Gardener, B.B. ; Thomashow, L.S. ; Weller, D.M. - \ 2002
Applied and Environmental Microbiology 68 (2002)7. - ISSN 0099-2240 - p. 3226 - 3237.
Indigenous populations of 2,4-diacetylphloroglucinol (2,4-DAPG)-producing fluorescent Pseudomonas spp. that occur naturally in suppressive soils are an enormous resource for improving biological control of plant diseases. Over 300 isolates of 2,4-DAPG-producing fluorescent Pseudomonas spp. were isolated from the rhizosphere of pea plants grown in soils that had undergone pea or wheat monoculture and were suppressive to Fusarium wilt or take-all, respectively. Representatives of seven genotypes, A, D, E, L, O, P, and Q, were isolated from both soils and identified by whole-cell repetitive sequence-based PCR (rep-PCR) with the BOXA1R primer, increasing by three (O, P, and Q) the number of genotypes identified previously among a worldwide collection of 2,4-DAPG producers. Fourteen isolates representing eight different genotypes were tested for their ability to colonize the rhizosphere of pea plants. Population densities of strains belonging to genotypes D and P were significantly greater than the densities of other genotypes and remained above log 6.0 CFU (g of root)-1 over the entire 15-week experiment. Genetic profiles generated by rep-PCR or restriction fragment length polymorphism analysis of the 2,4-DAPG biosynthetic gene phlD were predictive of the rhizosphere competence of the introduced 2,4-DAPG-producing strains.
Biocontrol Agents for Take-all
Raaijmakers, J.M. ; Weller, D.M. ; Thomashow, L.S. ; Cook, R.J. - \ 2002
Octrooinummer: US6447770, verleend: 2002-09-10.
Fluorescent Pseudomonas spp. are described which are effective for the control of diseases caused by the soil-borne fungus, Gaeumannomyces graminis (Gg), such as take-all, in small grain crops or turf grass. The subject biocontrol strains have a unique genotype as shown by a characteristic banding pattern, and exhibit root-colonizing ability which is characterized by both higher population density on roots and extended colonizing activity compared to known Gg-suppressive strains. A further property is the ability of a strain to duplicate the level of biocontrol obtained naturally in a take-all decline soil. Methods for isolation and identification of the strains and their use to control diseases caused by Gg are provided. In particular, strains of P. fluorescens NRRL B-21806 and NRRL B-21807.
|2,4-Diacetylphloroglucinol, a major determinant in the biological control of take-all disease of wheat
Thomashow, L.S. ; Mavrodi, O.V. ; Mavrodi, D.V. ; Raaijmakers, J.M. ; Bonsall, R.F. ; McSpadden-Gardener, B. ; Lee, Y.J. ; Park, M.J. ; Weller, D.M. - \ 2000
In: Biology of Plant-Microbe Interactions, volume 2 / P.J.G.M. de Wit, T. Bisseling, W.J. Stiekema (eds). - St. Paul, Minnesota, USA : International Society for Molecular Plant-Microbe Interactions, 2000. - ISBN 0-9654625-1-X - p. 331 - 335.
Genotypic and phenotypic diversity of phlD-containing Pseudomonas strains isolated from the rhizosphere of wheat
McSpadden Gardener, B.B. ; Schroeder, K.L. ; Kalloger, S.E. ; Raaijmakers, J.M. ; Thomashow, L.S. ; Weller, D.M. - \ 2000
Applied and Environmental Microbiology 66 (2000)5. - ISSN 0099-2240 - p. 1939 - 1946.
Production of 2,4-diacetylphloroglucinol (2,4-DAPG) in the rhizosphere by strains of fluorescent Pseudomonas spp. results in the suppression of root diseases caused by certain fungal plant pathogens. In this study, fluorescent Pseudomonas strains containing phlD, which is directly involved in the biosynthesis of 2,4-DAPG, were isolated from the rhizosphere of wheat grown in soils from wheat-growing regions of the United States and The Netherlands. To assess the genotypic and phenotypic diversity present in this collection, 138 isolates were compared to 4 previously described 2,4-DAPG producers. Thirteen distinct genotypes, one of which represented over 30␘f the isolates, were differentiated by whole-cell BOX-PCR. Representatives of this group were isolated from eight different soils taken from four different geographic locations. ERIC-PCR gave similar results overall, differentiating 15 distinct genotypes among all of the isolates. In most cases, a single genotype predominated among isolates obtained from each soil. Thirty isolates, representing all of the distinct genotypes and geographic locations, were further characterized. Restriction analysis of amplified 16S rRNA gene sequences revealed only three distinct phylogenetic groups, one of which accounted for 87␘f the isolates. Phenotypic analyses based on carbon source utilization profiles revealed that all of the strains utilized 49 substrates and were unable to grow on 12 others. Individually, strains could utilize about two-thirds of the 95 substrates present in Biolog SF-N plates. Multivariate analyses of utilization profiles revealed phenotypic groupings consistent with those defined by the genotypic analyses.
|Diversity and rhizosphere competence of 2,4-diacetylphloroglucinol (Phl)-producing Pseudomonas strains
Raaijmakers, J.M. ; Hayes, K. ; Thomashow, L.S. ; Weller, D.M. - \ 1999
Phytopathology 89 (1999)6 (supplement). - ISSN 0031-949X - p. S63 - S63.
|Genotypic and phenotypic diversity of PhlD-containing Pseudomonas
McSpadden Gardener, B. ; Schroeder, K. ; Kalloger, S. ; Raaijmakers, J. ; Thomashow, L. ; Weller, D. - \ 1999
In: Book of abstracts : 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam, the Netherlands, 25-30 July 1999. - [S.l.] : [s.n.], 1999 - p. 185 - 185.
|2 :4-diacetylphloroglucinol : a major determinant in the biological control of take-all disease of wheat
Mavrodi, O.V. ; Park, M.J. ; Mavrodi, D.V. ; Bonsall, R.F. ; Raaijmakers, J. ; Weller, D.M. ; Thomashow, L.S. - \ 1999
In: Book of abstracts : 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam, The Netherlands, 25-30 July 1999. - [S.l] : [s.n.], 1999 - p. 31 - 31.
|Improvement of activity against fungal wheat root diseases by transformation of phenazine biosynthetic genes into Pseudomonas fluorescens
Huang, Z. ; Mavrodi, D. ; Raaijmakers, J. ; Bonsall, R. ; Cook, R.J. ; Weller, D.M. ; Thomashow, L.S. - \ 1999
Phytopathology 89 (1999)6 (supplement). - ISSN 0031-949X - p. S35 - S35.
|The role of antibiotics in microbial interactions in the soil.
Weller, D.M. ; Raaijmakers, J.M. ; Thomashow, L.S. - \ 1998
In: 7th International Congress of Plant Pathology, Edinburgh, UK (1998) 2.7.5
|Molecular approaches to improve the efficacy of bacterial biocontrol agents.
Thomashow, L.S. ; Mavrodi, D.V. ; Huang, Z. ; Raaijmakers, J.M. ; Weller, D.M. - \ 1998
In: 7th International Congress of Plant Pathology, Edinburgh, UK (1998) 3.5.2
|Distribution of 2,4-diacetylphloroglucinol-producing Pseudomonas spp. with extended monoculture.
Schroeder, K.L. ; Raaijmakers, J.M. ; Kalloger, S.E. ; Mavrodi, D.V. ; Thomashow, L.S. ; Cook, R.J. ; Weller, D.M. - \ 1998
Phytopathology 88 (1998). - ISSN 0031-949X - p. 80 - 80.
|Diversity within phlD, a key gene in the biosynthesis of 2,4-diacetylphloroglucinol.
Mavrodi, O.V. ; Mavrodi, D.V. ; Raaijmakers, J.M. ; Schroeder, K.L. ; Kalloger, S.E. ; Weller, D.M. ; Thomashow, L.S. - \ 1998
Phytopathology 88 (1998). - ISSN 0031-949X - p. 59 - 59.
|The rhizosphere ecology of antibiotic-producing pseudomonads and their role in take-all decline.
Weller, D.M. ; Raaijmakers, J.M. ; Thomashow, L.S. - \ 1997
In: Plant Growth-Promoting Rhizobacteria: Present Status and Future Prospects / Ogoshi, A., - p. 58 - 64.
|2,4-diacetylphloroglucinol, a key antibiotic in soilborne pathogen suppression by fluorescent Pseudomonas spp.
Thomashow, L.S. ; Bangera, M.G. ; Bonsal, R.F. ; Kim, D.S. ; Raaijmakers, J.M. ; Weller, D.M. - \ 1997
In: Advances in molecular genetics of plant-microbe interactions - p. 469 - 475.
|Frequency of antibiotic-producing Pseudomonas spp. in natural environments.
Raaijmakers, J.M. ; Weller, D.M. ; Thomashow, L.S. - \ 1997
Applied and Environmental Microbiology 63 (1997). - ISSN 0099-2240 - p. 881 - 887.