Skip to main content
Log in

Dialogues of root-colonizing biocontrol pseudomonads

European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Among biocontrol agents that are able to suppress root diseases caused by fungal pathogens, root-colonizing fluorescent pseudomonads have received particular attention because many strains of these bacteria trigger systemic resistance in host plants and produce antifungal compounds and exoenzymes. In general, the expression of these plant-beneficial traits is regulated by autoinduction mechanisms and may occur on roots when the pseudomonads form microcolonies. Three major classes of antibiotic compounds reviewed here in detail (2,4-diacetylphloroglucinol, pyoluteorin and various phenazine compounds) are all produced under cell population density-dependent autoinduction control acting at transcriptional and post-transcriptional levels. This regulation can either be reinforced or attenuated by a variety of chemical signals emanating from the pseudomonads themselves, other microorganisms or root exudates. Signals stimulating biocontrol factor expression via the Gac/Rsm signal transduction pathway in the biocontrol strain Pseudomonas fluorescens CHA0 are synthesized by many different plant-associated bacteria, warranting a more detailed investigation in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

AHL:

N-acyl-homoserine lactone

AI-2:

Autoinducer 2

DAPG :

2,4-Diacetylphloroglucinol

HCN:

Hydrogen cyanide

IAA:

Indole-3-acetic acid

PCA:

Phenazine-1-carboxylic acid

PLT:

Pyoluteorin

PQS:

Pseudomonas quinolone signal

QS:

Quorum sensing

References

  • Abbas, A., McGuire, J. E., Crowley, D., Baysse, C., Dow, M., & O′Gara, F. (2004). The putative permease PhlE of Pseudomonas fluorescens F113 has a role in 2,4-diacetylphloroglucinol resistance and in general stress tolerance. Microbiology, 150, 2443–2450.

    PubMed  CAS  Google Scholar 

  • Achkar, J., Xian, M., Zhao, H., & Frost, J. W. (2005). Biosynthesis of phloroglucinol. Journal of the American Chemical Society, 127, 5332–5333.

    PubMed  CAS  Google Scholar 

  • Andersen, J. B., Koch, B., Nielsen, T. H., Sørensen, D., Hansen, M., Nybroe, O., Christophersen, C., Sørensen, J., Molin, S., & Givskov, M. (2003). Surface motility in Pseudomonas sp. DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum. Microbiology, 149, 1147–1156.

    Google Scholar 

  • Audenaert, K., Pattery, T., Cornelis, P., & Höfte, M. (2002). Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: Role of salicylic acid, pyochelin, and pyocyanin. Molecular Plant-Microbe Interactions, 15, 1147–1156.

    PubMed  CAS  Google Scholar 

  • Babitzke, P., & Romeo, T. (2007). CsrB sRNA family: Sequestration of RNA-binding regulatory proteins. Current Opinion in Microbiology, 10, 156–163.

    PubMed  CAS  Google Scholar 

  • Baehler, E., Bottiglieri, M., Péchy-Tarr, M., Maurhofer, M., & Keel, C. (2005). Use of green fluorescent protein-based reporters to monitor balanced production of antifungal compounds in the biocontrol agent Pseudomonas fluorescens CHA0. Journal of Applied Microbiology, 99, 24–38.

    PubMed  CAS  Google Scholar 

  • Baehler, E., de Werra, P., Wick, L. Y., Péchy-Tarr, M., Mathys, S., Maurhofer, M., & Keel, C. (2006). Two novel MvaT-like global regulators control exoproduct formation and biocontrol activity in root-associated Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions, 19, 313–329.

    PubMed  CAS  Google Scholar 

  • Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., & Vivanco, J. M. (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology, 57, 233–266.

    PubMed  CAS  Google Scholar 

  • Bangera, M. G., & Thomashow, L. S. (1999). Identification and characterization of a gene cluster for synthesis of the polyketide antibiotic 2,4-diacetylphloroglucinol from Pseudomonas fluorescens Q2-87. Journal of Bacteriology, 181, 3155–3163.

    PubMed  CAS  Google Scholar 

  • Bassler, B. L., Greenberg, E. P., & Stevens, A. M. (1997). Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. Journal of Bacteriology, 179, 4043–4045.

    PubMed  CAS  Google Scholar 

  • Bejerano-Sagie, M., & Xavier, K. B. (2007). The role of small RNAs in quorum sensing. Current Opinion in Microbiology, 10, 189–198.

    PubMed  CAS  Google Scholar 

  • Berg, G., Eberl, L., & Hartmann, A. (2005). The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environmental Microbiology, 7, 1673–1685.

    PubMed  CAS  Google Scholar 

  • Bertani, I., & Venturi, V. (2004). Regulation of the N-acyl homoserine lactone-dependent quorum-sensing system in rhizosphere Pseudomonas putida WCS358 and cross-talk with the stationary-phase RpoS sigma factor and the global regulator GacA. Applied and Environmental Microbiology, 70, 5493–5502.

    PubMed  CAS  Google Scholar 

  • Blumer, C., & Haas, D. (2000). Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Archives of Microbiology, 173, 170–177.

    PubMed  CAS  Google Scholar 

  • Blumer, C., Heeb, S., Pessi, G., & Haas, D. (1999). Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proceedings of the National Academy of Sciences USA, 96, 14073–14078.

    CAS  Google Scholar 

  • Bottiglieri, M., & Keel, C. (2006). Characterization of PhlG, a hydrolase that specifically degrades the antifungal compound 2,4-diacetylphloroglucinol in the biocontrol agent Pseudomonas fluorescens CHA0. Applied and Environmental Microbiology, 72, 418–427.

    PubMed  CAS  Google Scholar 

  • Brodhagen, M., Henkels, M. D., & Loper, J. E. (2004). Positive autoregulation and signaling properties of pyoluteorin, an antibiotic produced by the biological control organism Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology, 70, 1758–1766.

    PubMed  CAS  Google Scholar 

  • Brodhagen, M., Paulsen, I., & Loper, J. E. (2005). Reciprocal regulation of pyoluteorin production with membrane transporter gene expression in Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology, 71, 6900–6909.

    PubMed  CAS  Google Scholar 

  • Chancey, S. T., Wood, D. W., & Pierson, L. S. 3rd. (1999). Two-component transcriptional regulation of N-acyl-homoserine lactone production in Pseudomonas aureofaciens. Applied and Environmental Microbiology, 65, 2294–2299.

    PubMed  CAS  Google Scholar 

  • Chin-A-Woeng, T. F. C., Bloemberg, G. V., & Lugtenberg, B. J. J. (2003). Phenazines and their role in biocontrol by Pseudomonas bacteria. New Phytologist, 157, 503–523.

    CAS  Google Scholar 

  • Chin-A-Woeng, T. F. C., Thomas-Oates, J. E., Lugtenberg, B. J. J., & Bloemberg, G. V. (2001a). Introduction of the phzH gene of Pseudomonas chlororaphis PCL1391 extends the range of biocontrol ability of phenazine-1-carboxylic acid-producing Pseudomonas spp. strains. Molecular Plant-Microbe Interactions, 14, 1006–1015.

    PubMed  CAS  Google Scholar 

  • Chin-A-Woeng, T. F. C., van den Broek, D., de Voer, G., van der Drift, K., Tuinman, S., Thomas-Oates, J. E., Lugtenberg, B. J. J., & Bloemberg, G. V. (2001b). Phenazine-1-carboxamide production in the biocontrol strain Pseudomonas chlororaphis PCL1391 is regulated by multiple factors secreted into the growth medium. Molecular Plant-Microbe Interactions, 14, 969–979.

    PubMed  CAS  Google Scholar 

  • Compant, S., Duffy, B., Nowak, J., Clement, C., & Barka, E. A. (2005). Use of plant growth-promoting bacteria for biocontrol of plant diseases: Principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology, 71, 4951–4959.

    PubMed  CAS  Google Scholar 

  • Compeau, G., Al-Achi, B. J., Platsouka, E., & Levy, S. B. (1988). Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Applied and Environmental Microbiology, 54, 2432–2438.

    PubMed  CAS  Google Scholar 

  • de Souza, J. T., Arnould, C., Deulvot, C., Lemanceau, P., Gianinazzi-Pearson, V., & Raaijmakers, J. M. (2003b). Effect of 2,4-diacetylphloroglucinol on Pythium: Cellular responses and variation in sensitivity among propagules and species. Phytopathology, 93, 966–975.

    PubMed  Google Scholar 

  • de Souza, J. T., Weller, D. M., & Raaijmakers, J. M. (2003a). Frequency, diversity, and activity of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in Dutch take-all decline soils. Phytopathology, 93, 54–63.

    PubMed  Google Scholar 

  • de Vleesschauwer, D., Cornelis, P., & Höfte, M. (2006). Redox-active pyocyanin secreted by Pseudomonas aeruginosa 7HSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Molecular Plant-Microbe Interactions, 19, 1406–1419.

    PubMed  Google Scholar 

  • de Werra, P., Huser, A., Baehler, E., Keel, C., & Maurhofer, M. (2006). Using flow cytometry for in situ monitoring of antimicrobial compound production in the biocontrol bacterium Pseudomonas fluorescens CHA0. IOBC/WPRS Bulletin, 29, 117–121.

    Google Scholar 

  • Delaney, S. M., Mavrodi, D. V., Bonsall, R. F., & Thomashow, L. S. (2001). phzO, a gene for biosynthesis of 2-hydroxylated phenazine compounds in Pseudomonas aureofaciens 30-84. Journal of Bacteriology, 183, 318–327.

    PubMed  CAS  Google Scholar 

  • Delany, I., Sheehan, M. M., Fenton, A., Bardin, S., Aarons, S., & O’Gara, F. (2000). Regulation of production of the antifungal metabolite 2,4-diacetylphloroglucinol in Pseudomonas fluorescens F113: Genetic analysis of phlF as a transcriptional repressor. Microbiology, 146, 537–543.

    PubMed  CAS  Google Scholar 

  • Dietrich, L. E. P., Price-Whelan, A., Petersen, A., Whiteley, M., & Newman, D. K. (2006). The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Molecular Microbiology, 61, 1308–1321.

    PubMed  CAS  Google Scholar 

  • Dubuis, C. (2005). Cell-cell communication in the biocontrol strain Pseudomonas fluorescens CHA0. PhD thesis, Switzerland, Département de microbiologie fondamentale, University of Lausanne.

  • Dubuis, C., & Haas, D. (2007). Cross-species GacA-controlled induction of antibiosis in pseudomonads. Applied and Environmental Microbiology, 73, 650–654.

    PubMed  CAS  Google Scholar 

  • Dubuis, C., Rolli, J., Lutz, M., Défago, G., & Haas, D. (2006). Thiamine-auxotrophic mutants of Pseudomonas fluorescens CHA0 are defective in cell-cell signaling and biocontrol factor expression. Applied and Environmental Microbiology, 72, 2606–2613.

    PubMed  CAS  Google Scholar 

  • Duffy, B., & Défago, G. (1997). Zinc improves biocontrol of fusarium crown and root rot of tomato by Pseudomonas fluorescens and represses the production of pathogen metabolites inhibitory to bacterial antibiotic biosynthesis. Phytopathology, 87, 1250–1257.

    CAS  PubMed  Google Scholar 

  • Duffy, B., Keel, C., & Défago, G. (2004). Potential role of pathogen signaling in multitrophic plant-microbe interactions involved in disease protection. Applied and Environmental Microbiology, 70, 1836–1842.

    PubMed  CAS  Google Scholar 

  • Duffy, B., Schouten, A., & Raaijmakers, J. M. (2003). Pathogen self-defense: Mechanisms to counteract microbial antagonism. Annual Review of Phytopathology, 41, 501–538.

    PubMed  CAS  Google Scholar 

  • Fenton, A. M., Stephens, P. M., Crowley, J., O’Callaghan, M., & O’Gara, F. (1992). Exploitation of gene(s) involved in 2,4-diacetylphloroglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain. Applied and Environmental Microbiology, 58, 3873–3878.

    PubMed  CAS  Google Scholar 

  • Franklin, F. C., Bagdasarian, M., Bagdasarian, M. M., & Timmis, K. N. (1981). Molecular and functional analysis of the TOL plasmid pWWO from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta cleavage pathway. Proceedings of the National Academy of Sciences USA, 78, 7458–7462.

    CAS  Google Scholar 

  • Fuchs, J., & Défago, G. (1991). Protection of cucumber plants against black root rot caused by Phomopsis sclerotioides with rhizobacteria. In C. Keel, B. Koller, & G. Défago (Eds.), Plant growth-promoting rhizobacteria—progress and prospects (pp. 51–56). Interlaken, Switzerland: IOBC/WPRS.

    Google Scholar 

  • Fuqua, W. C., Winans, S. C., & Greenberg, E. P. (1994). Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. Journal of Bacteriology, 176, 269–275.

    PubMed  CAS  Google Scholar 

  • Gantner, S., Schmid, M., Dürr, C., Schuhegger, R., Steidle, A., Hutzler, P., Langebartels, C., Eberl, L., Hartmann, A., & Dazzo, F. B. (2006). In situ quantitation of the spatial scale of calling distances and population density-independent N-acylhomoserine lactone-mediated communication by rhizobacteria colonized on plant roots. FEMS Microbiology Ecology, 56, 188–194.

    PubMed  CAS  Google Scholar 

  • Gao, M., Teplitski, M., Robinson, J. B., & Bauer, W. D. (2003). Production of substances by Medicago trucatula that affect bacterial quorum sensing. Molecular Plant-Microbe Interactions, 16, 827–834.

    PubMed  CAS  Google Scholar 

  • Ge, Y., Huang, X., Wang, S., Zhang, X., & Xu, Y. (2004). Phenazine-1-carboxylic acid is negatively regulated and pyoluteorin positively regulated by GacA in Pseudomonas sp. M18. FEMS Microbiology Letters, 237, 41–47.

    PubMed  CAS  Google Scholar 

  • Gerritse, G., Hommes, R. W., & Quax, W. J. (1998). Development of a lipase fermentation process that uses a recombinant Pseudomonas alcaligenes strain. Applied and Environmental Microbiology, 64, 2644–2651.

    PubMed  CAS  Google Scholar 

  • Girard, G., Barends, S., Rigali, S., van Rij, E. T., Lugtenberg, B. J. J., & Bloemberg, G. V. (2006). Pip, a novel activator of phenazine biosynthesis in Pseudomonas chlororaphis PCL1391. Journal of Bacteriology, 188, 8283–8293.

    PubMed  CAS  Google Scholar 

  • González, J. E., & Keshavan, N. D. (2006). Messing with bacterial quorum sensing. Microbiology and Molecular Biology Reviews, 70, 859–875.

    PubMed  Google Scholar 

  • Goodman, A. L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R. S., & Lory, S. (2004). A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Developmental Cell, 7, 745–754.

    PubMed  CAS  Google Scholar 

  • Haas, D., Blumer, C., & Keel, C. (2000). Biocontrol ability of fluorescent pseudomonads genetically dissected: Importance of positive feedback regulation. Current Opinion in Biotechnology, 11, 290–297.

    PubMed  CAS  Google Scholar 

  • Haas, D., & Défago, G. (2005). Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology, 3, 307–319.

    PubMed  CAS  Google Scholar 

  • Haas, D., & Keel, C. (2003). Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annual Review of Phytopathology, 41, 117–153.

    PubMed  CAS  Google Scholar 

  • Haas D., Reimmann C., & Valverde, C. (2004). Common mechanisms in beneficial, deleterious host-microbe interactions. In L. Tikhonovich, B. Lugtenberg, & N. Provorov (Eds.), Biology of plant-microbe interactions (Vol. 4, pp. 537–541). St. Paul, Minnesota, USA: International Society for Molecular Plant-Microbe Interactions.

  • Han, S. H., Lee, S. J., Moon, J. H., Park, K. H., Yang, K. Y., Cho, B. H., Kim, K. Y., Kim, Y. W., Lee, M. C., Anderson, A. J., & Kim, Y. C. (2006). GacS-dependent production of 2R, 3R-butanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Molecular Plant-Microbe Interactions, 19, 924–930.

    PubMed  CAS  Google Scholar 

  • Harrison, L. A., Letendre, L., Kovacevich, P., Pierson, E., & Weller, D. (1993). Purification of an antibiotic effective against Gaeumannomyces graminis var. tritici produced by a biocontrol agent, Pseudomonas aureofaciens. Soil Biology and Biochemistry, 25, 215–221.

    CAS  Google Scholar 

  • Heeb, S., & Haas, D. (2001). Regulatory roles of the GacS/GacA two-component system in plant-associated and other Gram-negative bacteria. Molecular Plant-Microbe Interactions, 14, 1351–1363.

    PubMed  CAS  Google Scholar 

  • Hense, B. A., Kuttler, C., Müller, J., Rothballer, M., Hartmann, A., & Kreft, J.-U. (2007). Does efficiency sensing unify diffusion and quorum sensing? Nature Reviews Microbiology, 5, 230–239.

    PubMed  CAS  Google Scholar 

  • Hernandez, M. E., Kappler, A., & Newman, D. K. (2004). Phenazines and other redox-active antibioticx promote microbioal mineral reduction. Applied and Environmental Microbiology, 70, 921–928.

    PubMed  CAS  Google Scholar 

  • Heurlier, K., Williams, F., Heeb, S., Dormond, C., Pessi, G., Singer, D., Camara, M., Williams, P., & Haas, D. (2004). Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. Journal of Bacteriology, 186, 2936–2945.

    PubMed  CAS  Google Scholar 

  • Hirsch, A. M., Bauer, W. D., Bird, D. M., Cullimore, J., Tyler, A. B., & Yoderf, J. I. (2004). Molecular signals and receptors: Controlling rhizosphere interactions between plants and other organisms. Ecology, 84, 858–868.

    Google Scholar 

  • Holloway, B. W. (1955). Genetic recombination in Pseudomonas aeruginosa. Journal of General Microbiology, 13, 572–581.

    PubMed  CAS  Google Scholar 

  • Howell, C. R., & Stipanovic, R. D. (1980). Suppression of Pythium ultimum-induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Phytopathology, 70, 712–715.

    CAS  Google Scholar 

  • Huang, Z., Bonsall, R. F., Mavrodi, D. V., Weller, D., & Thomashow, L. S. (2003). Transformation of Pseudomonas fluorescens with genes for biosynthesis of phenazine-1-carboxylic acid improves biocontrol of rhizoctonia root rot and in situ antibiotic production. FEMS Microbiology Ecology, 49, 243–251.

    Google Scholar 

  • Huang, J. J., Petersen, A., Whiteley, M., & Leadbetter, J. R. (2006a). Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1. Applied and Environmental Microbiology, 72, 1190–1197.

    PubMed  CAS  Google Scholar 

  • Huang, X., Yan, A., Zhang, X., & Xu, Y. (2006b). Identification and characterization of a putative ABC transporter PltHIJKN required for pyoluteorin production in Pseudomonas sp. M18. Gene, 376, 68–78.

    PubMed  CAS  Google Scholar 

  • Huang, X., Zhu, D., Ge, Y., Hu, H., Zhang, X., & Xu, Y. (2004). Identification and characterization of pltZ, a gene involved in the repression of pyoluteorin biosynthesis in Pseudomonas sp. M18. FEMS Microbiology Letters, 232, 197–202.

    PubMed  CAS  Google Scholar 

  • Iavicoli, A., Boutet, E., Buchala, A., & Métraux, J. P. (2003). Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions, 16, 851–858.

    PubMed  CAS  Google Scholar 

  • Johansen, J. E., Binnerup, S. J., Lejbølle, K. B., Mascher, F., Sørensen, J., & Keel, C. (2002). Impact of biocontrol strain Pseudomonas fluorescens CHA0 on rhizosphere bacteria isolated from barley (Hordeum vulgare L.) with special reference to Cytophaga-like bacteria. Journal of Applied Microbiology, 93, 1065–1074.

    PubMed  CAS  Google Scholar 

  • Jousset, A., Lara, E., Wall, L. G., & Valverde, C. (2006). Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Applied and Environmental Microbiology, 72, 7083–7090.

    PubMed  CAS  Google Scholar 

  • Juhas, M., Eberl, L., & Tümmler, B. (2005). Quorum sensing: The power of cooperation in the world of Pseudomonas. Environmental Microbiology, 7, 459–471.

    PubMed  CAS  Google Scholar 

  • Kaur, R., Macleod, J., Foley, W., & Nayudu, M. (2006). Gluconic acid: An antifungal agent produced by Pseudomonas species in biological control of take-all. Phytochemistry, 67, 595–604.

    PubMed  CAS  Google Scholar 

  • Kay, E., Dubuis, C., & Haas, D. (2005). Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proceedings of the National Academy of Sciences USA, 102, 17136–17141.

    CAS  Google Scholar 

  • Kay, E., Humair, B., Dénervaud, V., Riedel, K., Spahr, S., Eberl, L., Valverde, C., & Haas, D. (2006). Two GacA-dependent small RNAs modulate the quorum sensing response in Pseudomonas aeruginosa. Journal of Bacteriology, 188, 6026–6033.

    PubMed  CAS  Google Scholar 

  • Keel, C., Schnider, U., Maurhofer, M., Voisard, C., Laville, J., Burger, U., Wirthner, P., Haas, D., & Défago, G. (1992). Suppression of root diseases by Pseudomonas fluorescens CHA0: Importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Molecular Plant-Microbe Interactions, 5, 4–13.

    CAS  Google Scholar 

  • Keel, C., Weller, D. M., Natsch, A., Défago, G., Cook, R. J., & Thomashow, L. S. (1996). Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas strains from diverse geographic locations. Applied and Environmental Microbiology, 62, 552–563.

    PubMed  CAS  Google Scholar 

  • Keel, C., Wirthner, P., Oberhänsli, T., Voisard, C., Burger, U., Haas, D., & Défago, G. (1990). Pseudomonads as antagonists of plant pathogens in the rhizosphere: Role of the antibiotic 2,4-diacetylphloroglucinol in the suppression of black root rot of tobacco. Symbiosis, 9, 327–341.

    CAS  Google Scholar 

  • Khan, S. R., Mavrodi, D. V., Jog, G. J., Suga, H., Thomashow, L. S., & Farrand, S. K. (2005). Activation of the phz operon of Pseudomonas fluorescens 2-79 requires the LuxR homolog PhzR, N-(3-OH-hexanoyl)-l-homoserine lactone produced by the LuxI homolog PhzI, and a cis-acting phz box. Journal of Bacteriology, 187, 6517–6527.

    PubMed  CAS  Google Scholar 

  • Kraus, J., & Loper, J. E. (1995). Characterization of a genomic region required for production of the antibiotic pyoluteorin by the biological control agent Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology, 61, 849–854.

    PubMed  CAS  Google Scholar 

  • Kuiper, I., Lagendijk, E. L., Pickford, R., Derrick, J. P., Lamers, G. E., Thomas-Oates, J. E., Lugtenberg, B. J. J., & Bloemberg, G. V. (2004). Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Molecular Microbiology, 51, 97–113.

    PubMed  CAS  Google Scholar 

  • Lakaye, B., Wirtzfeld, B., Wins, P., Grisar, T., & Bettendorff, L. (2004). Thiamine triphosphate, a new signal required for optimal growth of Escherichia coli during amino acid starvation. Journal of Biological Chemistry, 279, 17142–17147.

    PubMed  CAS  Google Scholar 

  • Laskowski, M. A., & Kazmierczak, B. I. (2006). Mutational analysis of RetS, an unusual sensor kinase-response regulator hybrid required for Pseudomonas aeruginosa virulence. Infection and Immunity, 74, 4462–4473.

    PubMed  CAS  Google Scholar 

  • Laue, B. E., Jiang, Y., Chhabra, S. R., Jacob, S., Stewart, G. S., Hardman, A., Downie, J. A., O’Gara, F., & Williams, P. (2000). The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl)-homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology, 146, 2469–2480.

    PubMed  CAS  Google Scholar 

  • Laville, J., Voisard, C., Keel, C., Maurhofer, M., Défago, G., & Haas, D. (1992). Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root rot of tobacco. Proceedings of the National Academy of Sciences USA, 89, 1562–1566.

    CAS  Google Scholar 

  • Lazdunski, A. M., Ventre, I., & Sturgis, J. N. (2004). Regulatory circuits and communication in Gram-negative bacteria. Nature Reviews Microbiology, 2, 581–592.

    PubMed  CAS  Google Scholar 

  • Lenz, D. H., Miller, M. B., Zhu, J., Kulkarni, R. V., & Bassler, B. L. (2005). CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Molecular Microbiology, 58, 1186–1202.

    PubMed  CAS  Google Scholar 

  • Ligon, J. M., Hill, D. S., Hammer, P. E., & Torkewitz, N. R. (1999). Genetic modifications of Pseudomonas that enhance biological disease control. Acta Horticulturae, 504, 53–60.

    Google Scholar 

  • Lugtenberg, B. J. J., & Bloemberg, G. V. (2004). Life in the rhizosphere. In J. L. Ramos (Ed.), Pseudomonas: Genomics, life style and molecular archtecture (Vol. 1, pp. 403–430). New York, NY, USA: Kluwer Academic/Plenum Publishers.

  • Lugtenberg, B. J. J., Dekkers, L., & Bloemberg, G. V. (2001). Molecular determinants of rhizosphere colonization by Pseudomonas. Annual Review of Phytopathology, 39, 461–490.

    PubMed  CAS  Google Scholar 

  • Lutz, M., Wenger, S., Maurhofer, M., Défago, G., & Duffy, B. (2004). Signaling between bacterial and fungal biocontrol agents in a strain mixture. FEMS Microbiology Ecology, 48, 447–455.

    CAS  PubMed  Google Scholar 

  • Maurhofer, M., Baehler, E., Notz, R., Martinez, V., & Keel, C. (2004). Cross talk between 2,4-diacetylphloroglucinol-producing biocontrol pseudomonads on wheat roots. Applied and Environmental Microbiology, 70, 1990–1998.

    PubMed  CAS  Google Scholar 

  • Maurhofer, M., Dubach, H., Haas, D., & Défago, G. (2002). How soilborne fungal pathogens affect the production of 2,4-diacetylphloroglucinol in biocontrol strain Pseudomonas fluorescens CHA0. IOBC/WPRS Bulletin, 25, 102–106.

    Google Scholar 

  • Maurhofer, M., Keel, C., Haas, D., & Défago, G. (1994). Pyoluteorin production by Pseudomonas fluorescens strain CHA0 is involved in the suppression of Pythium damping-off of cress but not of cucumber. European Journal of Plant Pathology, 100, 221–232.

    CAS  Google Scholar 

  • Maurhofer, M., Keel, C., Haas, D., & Défago, G. (1995). Influence of plant species on disease suppression by Pseudomonas fluorescens strain CHA0 with enhanced antibiotic production. Plant Pathology, 44, 40–50.

    Google Scholar 

  • Maurhofer, M., Keel, C., Schnider, U., Voisard, C., Haas, D., & Défago, G. (1992). Influence of enhanced antibiotic production in Pseudomonas fluorescens strain CHA0 on its disease suppressive capacity. Phytopathology, 82, 190–195.

    CAS  Google Scholar 

  • Mavrodi, D. V., Blankenfeldt, W., & Thomashow, L. S. (2006). Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annual Review of Phytopathology, 44, 417–445.

    PubMed  CAS  Google Scholar 

  • Mavrodi, D. V., Bonsall, R. F., Delaney, S. M., Soule, M. J., Phillips, G., & Thomashow, L. S. (2001). Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. Journal of Bacteriology, 183, 6454–6565.

    PubMed  CAS  Google Scholar 

  • Mavrodi, D. V., Ksenzenko, V. N., Bonsall, R. F., Cook, R. J., Boronin, A. M., & Thomashow, L. S. (1998). A seven-gene locus for synthesis is of phenazine-1-carboxylic acid by Pseudomonas fluorescens 2-79. Journal of Bacteriology, 180, 2541–2548.

    PubMed  CAS  Google Scholar 

  • Mazzola, M., Fujimoto, D. K., Thomashow, L. S., & Cook, R. J. (1995). Variation in sensitivity of Gaeumannomyces graminis to antibiotics produced by fluorescent Pseudomonas spp. and effect on biological control of take-all of wheat. Applied and Environmental Microbiology, 61, 2554–2559.

    PubMed  CAS  Google Scholar 

  • McClean, K. H., Winson, M. K., Fish, L., Taylor, A., Chhabra, S. R., Camara, M., Daykin, M., Lamb, J. H., Swift, S., Bycroft, B. W., Stewart, G. S., & Williams, P. (1997). Quorum sensing and Chromobacterium violaceum: Exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology, 143, 3703–3711.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, M., Mavrodi, D. V., Thomashow, L. S., & Floss, H. G. (2001). Phenazine biosynthesis in Pseudomonas fluorescens: Branchpoint from the primary shikimate biosynthetic pathway and role of phenazine-1,6-dicarboxylic acid. Journal of the American Chemical Society, 123, 9459–9460.

    PubMed  CAS  Google Scholar 

  • Moënne-Loccoz, Y., & Défago, G. (2004). Life as a biocontrol pseudomonad. In J. L. Ramos (Ed.), Pseudomonas: Genomics, life style and molecular archtecture (Vol. 1, pp. 457–476). New York, NY, USA: Kluwer Academic/Plenum Publishers.

    Google Scholar 

  • Molina, L., Constantinescu, F., Michel, L., Reimmann, C., Duffy, B., & Défago, G. (2003). Degradation of pathogen quorum-sensing molecules by soil bacteria: A preventive and curative biological control mechanism. FEMS Microbiology Ecology, 45, 71–81.

    CAS  PubMed  Google Scholar 

  • Morello, J. E., Pierson, E. A., & Pierson, L. S. 3rd. (2004). Negative cross-communication among wheat rhizosphere bacteria: Effect on antibiotic production by the biological control bacterium Pseudomonas aureofaciens 30-84. Applied and Environmental Microbiology, 70, 3103–3109.

    PubMed  CAS  Google Scholar 

  • Nealson, K. H. (1977). Autoinduction of bacterial luciferase. Occurrence, mechanism and significance. Archives of Microbiology, 112, 73–79.

    PubMed  CAS  Google Scholar 

  • Notz, R., Maurhofer, M., Dubach, H., Haas, D., & Défago, G. (2002). Fusaric acid-producing strains of Fusarium oxysporum alter 2,4-diacetylphloroglucinol biosynthetic gene expression in Pseudomonas fluorescens CHA0 in vitro and in the rhizosphere of wheat. Applied and Environmental Microbiology, 68, 2229–2235.

    PubMed  CAS  Google Scholar 

  • Notz, R., Maurhofer, M., Schnider-Keel, U., Duffy, B., Haas, D., & Défago, G. (2001). Biotic factors affecting expression of the 2,4-diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology, 91, 873–881.

    CAS  PubMed  Google Scholar 

  • Nowak-Thompson, B., Chaney, N., Wing, J. S., Gould, S. J., & Loper, J. E. (1999). Characterization of the pyoluteorin biosynthetic gene cluster of Pseudomonas fluorescens Pf-5. Journal of Bacteriology, 181, 2166–2174.

    PubMed  CAS  Google Scholar 

  • Parsons, J. F., Greenhagen, B. T., Shi, K., Calabrese, K., Robinson, H., & Ladner, J. E. (2007). Structural and functional analysis of the pyocyanin biosynthetic protein PhzM from Pseudomonas aeruginosa. Biochemistry, 46, 1821–1828.

    PubMed  CAS  Google Scholar 

  • Paulsen, I. T., Press, C. M., Ravel, J., Kobayashi, D. Y., Myers, G. S., Mavrodi, D. V., DeBoy, R. T., Seshadri, R., Ren, Q., Madupu, R., Dodson, R. J., Durkin, A. S., Brinkac, L. M., Daugherty, S. C., Sullivan, S. A., Rosovitz, M. J., Gwinn, M. L., Zhou, L., Schneider, D. J., Cartinhour, S. W., Nelson, W. C., Weidman, J., Watkins, K., Tran, K., Khouri, H., Pierson, E. A., Pierson, L. S. 3rd, Thomashow, L. S., & Loper, J. E. (2005). Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nature Biotechnology, 23, 873–878.

    PubMed  CAS  Google Scholar 

  • Péchy-Tarr, M., Bottiglieri, M., Mathys, S., Bang-Lejbølle, K., Schnider-Keel, U., Maurhofer, M., & Keel, C. (2005). RpoN (sigma54) controls production of antifungal compounds and biocontrol activity in Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions, 18, 260–272.

    PubMed  Google Scholar 

  • Pessi, G., Williams, F., Hindle, Z., Heurlier, K., Holden, M. T., Camara, M., Haas, D., & Williams, P. (2001). The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. Journal of Bacteriology, 183, 6676–6683.

    PubMed  CAS  Google Scholar 

  • Phillips, D. A., Fox, T. C., King, M. D., Bhuvaneswari, T. V., & Teuber, L. R. (2004). Microbial products trigger amino acid exudation from plant roots. Plant Physiology, 136, 2887–2894.

    PubMed  CAS  Google Scholar 

  • Phillips, D. A., & Kapulnik, Y. (1995). Plant isoflavonoids, pathogens and symbionts. Trends in Microbiology, 3, 58–64.

    PubMed  CAS  Google Scholar 

  • Pierson, L. S. 3rd, Gaffney, T., Lam, S., & Gong, F. (1995). Molecular analysis of genes encoding phenazine biosynthesis in the biological control bacterium. Pseudomonas aureofaciens 30-84. FEMS Microbiology Letters, 134, 299–307.

    PubMed  CAS  Google Scholar 

  • Pierson, E. A., & Weller, D. M. (1994). Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. Phytopathology, 84, 940–947.

    Google Scholar 

  • Pierson, L. S. 3rd, Wood, D. W., & Pierson, E. A. (1998). Homoserine lactone-mediated gene regulation in plant-associated bacteria. Annual Review of Phytopathology, 36, 207–225.

    PubMed  CAS  Google Scholar 

  • Price-Whelan, A., Dietrich, L. E., & Newman, D. K. (2006). Rethinking ‘secondary’ metabolism: Physiological roles for phenazine antibiotics. Nature Chemical Biology, 2, 71–78.

    PubMed  CAS  Google Scholar 

  • Prithiviraj, B., Bais, H. P., Weir, T., Suresh, B., Najarro, E. H., Dayakar, B. V., Schweizer, H. P., & Vivanco, J. M. (2005). Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infection and Immunity, 73, 5319–5328.

    PubMed  CAS  Google Scholar 

  • Quay, S. C., Friedman, S. B., & Eisenberg, R. C. (1972). Gluconate regulation of glucose catabolism in Pseudomonas fluorescens. Journal of Bacteriology, 112, 291–298.

    PubMed  CAS  Google Scholar 

  • Raaijmakers, J. M., de Bruijn, I., & de Kock, M. J. D. (2006). Cyclic lipopeptide production by plant-associated Pseudomonas spp.: Diversity, activity, biosynthesis, and regulation. Molecular Plant-Microbe Interactions, 19, 699–710.

    PubMed  CAS  Google Scholar 

  • Raaijmakers, J. M., Vlami, M., & de Souza, J. T. (2002). Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek, 81, 537–547.

    PubMed  CAS  Google Scholar 

  • Rainey, P. B., & Bailey, M. J. (1996). Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome. Molecular Microbiology, 19, 521–533.

    PubMed  CAS  Google Scholar 

  • Ramette, A., Moënne-Loccoz, Y., & Défago, G. (2003). Prevalence of fluorescent pseudomonads producing antifungal phloroglucinols and/or hydrogen cyanide in soils naturally suppressive or conducive to tobacco black root rot. FEMS Microbiology Ecology, 44, 35–43.

    CAS  PubMed  Google Scholar 

  • Rasmussen, T. B., Skindersoe, M. E., Bjarnsholt, T., Phipps, R. K., Christensen, K. B., Jensen, P. O., Andersen, J. B., Koch, B., Larsen, T. O., Hentzer, M., Eberl, L., Høiby, N., & Givskov, M. (2005). Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology, 151, 1325–1340.

    PubMed  CAS  Google Scholar 

  • Reimmann, C., Beyeler, M., Latifi, A., Winteler, H., Foglino, M., Lazdunski, A., & Haas, D. (1997). The global activator GacA of Pseudomonas aeruginosa PAO1 positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Molecular Microbiology, 24, 309–319.

    PubMed  CAS  Google Scholar 

  • Reimmann, C., Valverde, C., Kay, E., & Haas, D. (2005). Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHA0. Journal of Bacteriology, 187, 276–285.

    PubMed  CAS  Google Scholar 

  • Rezzonico, F., Zala, M., Keel, C., Duffy, B., Moënne-Loccoz, Y. & Défago, G. (2007). Is the ability of biocontrol fluorescent pseudomonads to produce the antifungal metabolite 2,4-diacetylphloroglucinol really synonymous with higher plant protection? New Phytologist, 173, 861–872.

    PubMed  CAS  Google Scholar 

  • Riedel, K., Hentzer, M., Geisenberger, O., Huber, B., Steidle, A., Wu, H., Hoiby, N., Givskov, M., Molin, S., & Eberl, L. (2001). N-Acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology, 147, 3249–3262.

    PubMed  CAS  Google Scholar 

  • Sambrook, J., & Russell, D. W. (2001). Molecular cloning: A laboratory manual (3rd ed.). Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Sarniguet, A., Kraus, J., Henkels, M. D., Muehlchen, A. M. & Loper, J. E. (1995). The sigma factor sigma s affects antibiotic production and biological control activity of Pseudomonas fluorescens Pf-5. Proceedings of the National Academy of Sciences USA, 92, 12255–12259.

    CAS  Google Scholar 

  • Schmidli-Sacherer, P., Keel, C., & Défago, G. (1997). The global regulator GacA of Pseudomonas fluorescens CHA0 is required for suppression of root diseases in dicotyledons but not in Gramineae. Plant Pathology, 46, 80–90.

    CAS  Google Scholar 

  • Schnider, U., Keel, C., Blumer, C., Troxler, J., Défago, G., & Haas, D. (1995). Amplification of the housekeeping sigma factor in Pseudomonas fluorescens CHA0 enhances antibiotic production and improves biocontrol abilities. Journal of Bacteriology, 177, 5387–5392.

    PubMed  CAS  Google Scholar 

  • Schnider-Keel, U., Seematter, A., Maurhofer, M., Blumer, C., Duffy, B., Gigot-Bonnefoy, C., Reimmann, C., Notz, R., Défago, G., Haas, D., & Keel, C. (2000). Autoinduction of 2,4-diacetylphloroglucinol biosynthesis in the biocontrol agent Pseudomonas fluorescens CHA0 and repression by the bacterial metabolites salicylate and pyoluteorin. Journal of Bacteriology, 182, 1215–1225.

    PubMed  CAS  Google Scholar 

  • Schouten, A., van den Berg, G., Edel-Hermann, V., Steinberg, C., Gautheron, N., Alabouvette, C., de Vos, C. H., Lemanceau, P., & Raaijmakers, J. M. (2004). Defense responses of Fusarium oxysporum to 2,4-diacetylphloroglucinol, a broad-spectrum antibiotic produced by Pseudomonas fluorescens. Molecular Plant-Microbe Interactions, 17, 1201–1211.

    PubMed  CAS  Google Scholar 

  • Sharifi-Tehrani, A., Zala, M., Natsch, A., Moënne-Loccoz, Y., & Défago, G. (1998). Biocontrol of soilborne fungal plant diseases by 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas with different restriction profiles of amplified 16S rDNA. European Journal of Plant Pathology, 104, 631–643.

    CAS  Google Scholar 

  • Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E. Jr., Rinehart, K. L., & Farrand, S. K. (1997). Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proceedings of the National Academy of Sciences USA, 94, 6036–6041.

    CAS  Google Scholar 

  • Siddiqui, I. A., Haas, D., & Heeb, S. (2005). Extracellular protease of Pseudomonas fluorescens CHA0, a biocontrol factor with activity against the root-knot nematode Meloidogyne incognita. Applied and Environmental Microbiology, 71, 5646–5649.

    PubMed  CAS  Google Scholar 

  • Siqueira, J. O., Nair, M. G., Hammerschmidt, R., & Safir, G. R. (1991). Significance of phenolic compounds in plant-soil-microbial systems. Critical Reviews in Plant Sciences, 10, 63–121.

    CAS  Google Scholar 

  • Somers, E., Vanderleyden, J., & Srinivasan, M. (2004). Rhizosphere bacterial signalling: A love parade beneath our feet. Critical Reviews in Microbiology, 30, 205–240.

    PubMed  CAS  Google Scholar 

  • Steidle, A., Sigl, K., Schuhegger, R., Ihring, A., Schmid, M., Gantner, S., Stoffels, M., Riedel, K., Givskov, M., Hartmann, A., Langebartels, C., & Eberl, L. (2001). Visualization of N-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Applied and Environmental Microbiology, 67, 5761–5770.

    PubMed  CAS  Google Scholar 

  • Stutz, E. W., Défago, G., & Kern, H. (1986). Naturally occurring fluorescent pseudomonads involved in suppression of black root rot of tobacco. Phytopathology, 76, 181–185.

    Google Scholar 

  • Sutra, L., Siverio, F., Lopez, M. M., Hunault, G., Bollet, C., & Gardan, L. (1997). Taxonomy of Pseudomonas strains isolated from tomato pith necrosis: Amended description of Pseudomonas corrugata and proposal of three unnamed fluorescent Pseudomonas genomospecies. International Journal of Systematic Bacteriology, 47, 1020–1033.

    Article  PubMed  CAS  Google Scholar 

  • Thomashow, L. S., & Weller, D. M. (1988). Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. Journal of Bacteriology, 170, 3499–3508.

    PubMed  CAS  Google Scholar 

  • Troxler, J., Azelvandre, P., Zala, M., Défago, G., & Haas, D. (1997). Conjugative transfer of chromosomal genes between fluorescent pseudomonads in the rhizosphere of wheat. Applied and Environmental Microbiology, 63, 213–219.

    PubMed  CAS  Google Scholar 

  • Turner, P., Barber, C., & Daniels, M. (1984). Behavior of the transposon Tn5 and Tn7 in Xanthomonas campestris pv. campestris. Molecular and General Genetics, 195, 101–107.

    CAS  Google Scholar 

  • van den Broek, D., Chin-A-Woeng, T. F. C., Eijkemans, K., Mulders, I. H. M., Bloemberg, G. V., & Lugtenberg, B. J. J. (2003). Biocontrol traits of Pseudomonas spp. are regulated by phase variation. Molecular Plant-Microbe Interactions, 16, 1003–1012.

    PubMed  Google Scholar 

  • van Loon, L. C., Bakker, P. A. H. M., & Pieterse, C. M. J. (1998). Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology, 36, 453–483.

    PubMed  Google Scholar 

  • van Rij, E. T., Girard, G., Lugtenberg, B. J. J., & Bloemberg, G. V. (2005). Influence of fusaric acid on phenazine-1-carboxamide synthesis and gene expression of Pseudomonas chlororaphis strain PCL1391. Microbiology, 151, 2805–2814.

    PubMed  Google Scholar 

  • Ventre, I., Goodman, A. L., Vallet-Gely, I., Vasseur, P., Soscia, C., Molin, S., Bleves, S., Lazdunski, A., Lory, S., Filloux, A. (2006). Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proceedings of the National Academy of Sciences USA, 103, 171–176.

    CAS  Google Scholar 

  • Wang, C., Zhang, H. B., Wang, L. H., & Zhang, L. H. (2006). Succinic semialdehyde couples stress response to quorum-sensing signal decay in Agrobacterium tumefaciens. Molecular Microbiology, 62, 45–56.

    PubMed  CAS  Google Scholar 

  • Wei, H. L., & Zhang, L. Q. (2006). Quorum-sensing system influences root colonization and biological control ability in Pseudomonas fluorescens 2P24. Antonie van Leeuwenhoek, 267–280, 1–14.

    Google Scholar 

  • Weller, D. M. (1983). Colonization of wheat roots by a fluorescent pseudomonad suppressive to take-all. Phytopathology, 73, 1548–1553.

    Article  Google Scholar 

  • Weller, D. M., Landa, B. B., Mavrodi, O. V., Schroeder, K. L., De La Fuente, L., Blouin Bankhead, S., Allende Molar, R., Bonsall, R. F., Mavrodi, D. V., & Thomashow, L. S. (2007). Role of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biology, 9, 4–20.

    PubMed  CAS  Google Scholar 

  • Weller, D. M., Raaijmakers, J. M., Gardener, B. B., & Thomashow, L. S. (2002). Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology, 40, 309–348.

    PubMed  CAS  Google Scholar 

  • Whistler, C. A., & Pierson, L. S. 3rd. (2003). Repression of phenazine antibiotic production in Pseudomonas aureofaciens strain 30-84 by RpeA. Journal of Bacteriology, 185, 3718–3725.

    PubMed  CAS  Google Scholar 

  • Whistler, C. A., Stockwell, V. O., & Loper, J. E. (2000). Lon protease influences antibiotic production and UV tolerance of Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology, 66, 2718–2725.

    PubMed  CAS  Google Scholar 

  • Winzer, K., Hardie, K. R., & Williams, P. (2002). Bacterial cell-to-cell communication: Sorry, can’t talk now—gone to lunch! Current Opinion in Microbiology, 5, 216–222.

    PubMed  CAS  Google Scholar 

  • Wood, D. W., Gong, F., Daykin, M., Williams, P., & Pierson, L. S. (1997). N-Acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30-84 in the wheat rhizosphere. Journal of Bacteriology, 179, 7663–7670.

    PubMed  CAS  Google Scholar 

  • Wood, D. W., & Pierson, L. S. (1996). The phzI gene of Pseudomonas aureofaciens 30-84 is responsible for the production of a diffusible signal required for phenazine antibiotic production. Gene, 168, 49–53.

    PubMed  CAS  Google Scholar 

  • Xavier, K. B., & Bassler, B. L. (2005). Interference with AI-2-mediated bacterial cell-cell communication. Nature, 437, 750–753.

    PubMed  CAS  Google Scholar 

  • Yahr, T. L., & Wolfgang, M. C. (2006). Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Molecular Microbiology, 62, 631–640.

    PubMed  CAS  Google Scholar 

  • Zha, W., Rubin-Pitel, S. B., & Zhao, H. (2006). Characterization of the substrate specificity of PhlD, a type III polyketide synthase from Pseudomonas fluorescens. Journal of Biological Chemistry, 281, 32036–32047.

    PubMed  CAS  Google Scholar 

  • Zhang, L. H., & Dong, Y. H. (2004). Quorum sensing and signal interference: Diverse implications. Molecular Microbiology, 53, 1563–1571.

    PubMed  CAS  Google Scholar 

  • Zuber, S., Carruthers, F., Keel, C., Mattart, A., Blumer, C., Pessi, G., Gigot-Bonnefoy, C., Schnider-Keel, U., Heeb, S., Reimmann, C., & Haas, D. (2003). GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions, 16, 634–644.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge financial support from the Swiss National Science Foundation (projects 3100A0-100180 and 3100A0-105881) and from the State Secretariat for Education and Research (COST project C04.0201).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dieter Haas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dubuis, C., Keel, C. & Haas, D. Dialogues of root-colonizing biocontrol pseudomonads. Eur J Plant Pathol 119, 311–328 (2007). https://doi.org/10.1007/s10658-007-9157-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-007-9157-1

Keywords

Navigation