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Plant disease and pest insect control by beneficial bacteria

Description | Bibliography (selected publications)
 

Description

Interactions between Pseudomonas fluorescens, phytopathogenic fungi, and crop plants. Soil-borne fungal pathogens attack plant roots and cause important damage to crop health. Environmental and public health concerns restrict the use of pesticides in soil to control these root diseases. The treatment of soil or planting material with certain strains of plant-beneficial, root-colonizing Pseudomonas spp. is a promising alternative to control root diseases. Control of root diseases by beneficial pseudomonads involves a blend of possible mechanisms that may complement each other. Direct antagonism against the pathogen by production of diffusible or volatile antibiotic compounds or by inactivation of virulence traits of the pathogen is considered to be a primary mechanism of biocontrol. Another important mechanism is the indirect inhibition of the pathogen by bacterial stimulation of defence responses in the plant host. In our work, we rely on the model bacterium P. fluorescens strain CHA0 which displays a remarkably broad spectrum of biocontrol activity against some of the major soil-borne plant pathogens on various mono- and dicotyledonous crop plants. Remarkably, strain CHA0 while colonizing only the roots can also provide plant protection against leaf pathogens by triggering systemic defense mechanisms.

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Regulation of antibiotic production in P. fluorescens. There is compelling evidence for a determinative role of Pseudomonas antibiotics in disease suppression. Some strains such as P. fluorescens CHA0 produce multiple antibiotics with overlapping or different degrees of activity against specific pathogens. Antifungal compounds excreted by strain CHA0 include 2,4-diacetylphloroglucinol (DAPG), pyoluteorin (PLT), pyrrolnitrin, and hydrogen cyanide. In recent years, we have identified biosynthetic and regulatory loci required for the production of these antibiotics. Besides pathway-specific regulators, a number of global regulatory elements are involved in the control of the biosyntheses of these compounds, among them the sigma factors RpoD, RpoS and RpoN, and a two-component system composed of the sensor kinase GacS and the response regulator GacA. In addition, numerous biotic and abiotic signals may also influence the production of these antifungal compounds, including different mineral and carbon sources as well as metabolites released by microorganisms and plants. Recently, we have obtained evidence that strain CHA0 keeps the antibiotics DAPG and PLT at a fine-tuned balance that can be affected by certain microbial and plant phenolics. We have developed a reporter system based on autofluorescent green (GFP) and red (DsRed) proteins to monitor changes in the balance of DAPG and PLT expression in the rhizosphere of healthy and pathogen-attacked plants. In situ monitoring of antibiotic gene expression involves the use of flow cytometry and fluorescence microscopy. We expect to get more insight into signalling events in the rhizosphere that critically influence the balance of antibiotic production, thereby affecting biocontrol activity and competitive behavior of P. fluorescens.

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Insecticidal activity in root associated pseudomonads. Recently, we discovered that some of the root-associated Pseudomonas strains also exhibit potent insecticidal activity. Anti-insect activity is due, in part, to the production of a novel protein toxin that is related to insect toxins produced by entomopathogenic bacteria associated with insect-invading nematodes. The occurrence of antifungal and anti-insect activities in root-colonizing pseudomonads highlights not only the impressive arsenal of features that these bacteria possess to manipulate their rhizosphere habitat, but points also to new possibilities to protect the health of agricultural crops. In our current work, we wish to learn more about the ecological function of the insect toxin and the other Pseudomonas exoproducts in the plant root environment and we try to identify regulatory elements and signals that control their production and biological activity.  

Bibliography (selected publications)

  1. Keel, C., Weller, D. M., Natsch, A., Défago, G., Cook, R. J., and Thomashow, L. S. 1996. Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas strains from diverse geographic locations. Appl. Environ. Microbiol. 62: 552-563.

  2. Keel, C., and Défago, G. 1997. Interactions between beneficial soil bacteria and root pathogens: mechanisms and ecological impact, pp. 27-46. In A. C. Gange and V. K. Brown (eds.), Multitrophic Interactions in Terrestrial Systems. Blackwell Science, London.

  3. Haas, D., Blumer, C., and Keel, C. 2000. Biocontrol ability of fluorescent pseudomonads genetically dissected: importance of positive feedback regulation. Curr. Opin. Biotechnol. 11: 290-297.

  4. Schnider-Keel, U., Seematter, A., Maurhofer, M., Blumer, C., Duffy, B., Gigot-Bonnefoy, C., Reimmann, C., Notz, R., Défago, G., Haas, D., and 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. J. Bacteriol. 182: 1215-1225.

  5. Schnider-Keel, U., Bang Lejbølle, K., Baehler, E., Haas, D., and Keel, C. 2001. The sigma factor AlgU (AlgT) controls exopolysaccharide production and tolerance towards desiccation and osmotic stress in the biocontrol agent Pseudomonas fluorescens CHA0. Appl. Environ. Microbiol. 67: 5683-5693.

  6. Keel, C., Ucurum, Z., Michaux, M., Adrian, M., and Haas, D. 2002. Deleterious impact of a virulent bacteriophage on survival and biocontrol activity of Pseudomonas fluorescens strain CHA0 in natural soil. Mol. Plant-Microbe Interact. 15: 567-576.

  7. Smits, T. H. M., Wick, L. Y., Harms, H., and Keel, C. 2002. Characterization of the surface hydrophobicity of filamentous fungi. Environ. Microbiol. 5: 85-91.

  8. Haas, D., and Keel, C. 2003. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu. Rev. Phytopathol. 41: 117-153.

  9. Maurhofer, M., Baehler, E., Notz, R. Martinez, V., and Keel, C. 2004. Cross talk between 2,4-diacetylphloroglucinol-producing biocontrol pseudomonads on wheat roots. Appl. Environ. Microbiol. 70: 1990-1998.

  10. Péchy-Tarr, M., Bottiglieri, M., Mathys, S., Lejbølle, K. B., Schnider-Keel, U., Maurhofer, M., and Keel, C. 2005. RpoN (sigma-54) controls production of antifungal compounds and biocontrol activity in Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 18: 260-272.

  11. Baehler, E., Bottiglieri, M., Péchy-Tarr, M., Maurhofer, M., and Keel, C. 2005. Use of green fluorescent protein-based reporters to monitor balanced production of antifungal compounds in the biocontrol agent Pseudomonas fluorescens CHA0. J. Appl. Microbiol. 99: 24-38.

  12. Bottiglieri, M., and Keel, C. 2006. Characterization of PhlG, a hydrolase that specifically degrades the antifungal compound 2,4-diacetylphloroglucinol in the biocontrol agent Pseudomonas fluorescens CHA0. Appl. Environ. Microbiol. 72:418-427.

  13. Baehler, E., de Werra, P., Wick, L. Y., Péchy-Tarr, M., Mathys, S., Maurhofer, M., and Keel, C. 2006. Two novel MvaT-like global regulators control exoproduct formation and biocontrol activity in root-associated Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 19: 313-329.

  14. De Werra, P., Baehler, E., Huser, A., Keel, C., Maurhofer, M. 2008 Detection of plant-modulated alterations in antifungal gene expression by Pseudomonas fluorescens CHA0 on roots by flow cytometry. Appl. Environ. Microbiol. 74: 1339-1349.

  15. Péchy-Tarr, M., Bruck, D.J., Maurhofer, M., Fischer, E., Vogne, C., Henkels, M.D., Donahue, K.M., Grunder, J., Loper, J.E., and Keel, C. 2008. Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ. Microbiol. 10: 2368-2386.

  16. Jousset, A., Rochat, L., Péchy-Tarr, M., Keel, C., Scheu, S., and Bonkowski, M. 2009. Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters. ISME J. 3: 666-674.

  17. de Werra, P., Péchy-Tarr, M., Keel, C., and Maurhofer, M. 2009. Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0. Appl. Environ. Microbiol. 75: 4162-4174.

  18. Bjørnlund, L., Rønn, R., Péchy-Tarr, M., Maurhofer, M., Keel, C., and Nybroe, O. 2009. Functional GacS in Pseudomonas DSS73 prevents digestion by Caenorhabditis elegans and protects the nematode from killer flagellates. ISME J. 3: 770-779.

  19. Scheublin, T.R., Sanders, I., Keel, C., and van der Meer, J.R. 2010. Characterisation of microbial communities colonising the hyphal surfaces of arbuscular mycorrhizal fungi. ISME J. 4: 752-763.

  20. Vallet-Gely, I, Novikov, A, Augusto, L, Liehl, P, Bolbach, G, Péchy-Tarr, M, Cosson, P, Keel, C, Caroff, M, and Lemaitre, B. 2010. Association of hemolytic activity of Pseudomonas entomophila, a versatile soil bacterium, with cyclic lipopeptide production. Appl. Environ. Microbiol. 76: 910-921.

  21. Rochat, L., Péchy-Tarr, M., Baehler E., Maurhofer, M., and Keel C. 2010. Combination of fluorescent reporters for simultaneous monitoring of root colonization and antifungal gene expression by a biocontrol pseudomonad on cereals with flow cytometry. Mol. Plant-Microbe Interact. 23: 949-961.

  22. Jousset, A., Rochat, L., Scheu, S., Bonkowski, M., and Keel C. 2010. Predator-prey chemical warfare determines the expression of biocontrol genes by rhizosphere pseudomonads. Appl Environ Microbiol. 76: 5263-5268.

  23. Meyer J.B., Lutz M.P., Frapolli M., Péchy-Tarr M., Rochat L., Keel C., Défago G., Maurhofer M. 2010. Interplay between wheat cultivars, biocontrol pseudomonads, and soil. Appl. Environ. Microbiol. 76: 6196-204.

  24. Jousset, A., Rochat, L., Lanoue, A., Bonkowski, M., Keel, C. and Scheu, S. 2011. Plants respond to pathogen infections by enhancing the antifungal gene expression of root-associated bacteria. Mol. Plant-Microbe Interact. 24: 352-358.

  25. Subramoni S., Gonzalez J.F., Johnson A., Péchy-Tarr M., Rochat L., Paulsen I., Loper J.E., Keel C., Venturi V. 2011. Bacterial subfamily of LuxR regulators that respond to plant compounds. Appl. Environ. Microbiol. 77: 4579-88.

  26. de Werra P., Huser A., Tabacchi R., Keel C., Maurhofer M. 2011. Plant- and microbe-derived compounds affect the expression of genes encoding antifungal compounds in a pseudomonad with biocontrol activity. Appl. Environ. Microbiol. 77: 2807-12.

  27. Meyer J.B., Frapolli M., Keel C., Maurhofer M. 2011. Pyrroloquinoline quinone biosynthesis gene pqqC, a novel molecular marker for studying the phylogeny and diversity of phosphate-solubilizing pseudomonads. Appl. Environ. Microbiol. 77: 7345-54.

  28. Troxler J., Svercel M., Natsch A., Zala M., Keel C., Moënne-Loccoz Y., Défago G. 2012. Persistence of a biocontrol Pseudomonas inoculant as high populations of culturable and non-culturable cells in 200-cm-deep soil profiles. Soil Biol. Biochem. 44: 122-9.

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Group leader

Senior researcher

Dr. Maria Péchy-Tarr

Post-Doc

PhD students

Peter Kupferschmied
Joana Meyer (ETH Zürich, common project Dr. M. Maurhofer)

Master students

Nicola Imperiali
Nicolo Tosetti
Raphaël Groux

Scientific collaborators

Karent Paola Bermudez Valdes

Former scientific collaborators

Jérôme Wassef
Jérémy Pittet

Biophore - CH-1015 Lausanne  - Switzerland  -  Tel. +41 21 692 56 00  -  Fax +41 21 692 56 05
Swiss University