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Microbe–plant interactions: principles and mechanisms

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Abstract

The present status of research on the molecular basis of microbe–plant interactions is discussed. Principles and mechanisms which play a role in the interactions of microbial pathogens, biofertilizers, phytostimulators, rhizoremediators and biocontrol agents with the plants are treated. Special emphasis is given to colonization, phase variation, two-component systems, quorum sensing, complex regulation of the syntheses of extracellular enzymes and secondary metabolites, Type 4 pili and Type III and Type IV secretion systems.

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References

  • Aarons S, Abbas A, Adams C, Fenton A & O'Gara F (2000) A regulatory RNA (PrrB RNA) modulates expression of secondary metabolite genes in Pseudomonas fluorescens F113. J. Bacteriol. 182: 3913–3919.

    Article  PubMed  CAS  Google Scholar 

  • Alabouvette C (1986) Fusarium wilt suppresive soils from the chateaurenard region: review of a 10 year study. Agronomie 6: 273–284.

    Google Scholar 

  • Allaway D, Schofield NA, Leonard ME, Gilardoni L, Finan TM & Poole PS (2001) Use of differential fluorescence induction and optical trapping to isolate environmentally induced genes. Environ. Microbiol. 3: 397–406.

    Article  PubMed  CAS  Google Scholar 

  • Bakker PAHM, van Peer R & Schippers B (1990) In: Hornby D (Ed) Biological Control of Soil-Borne Plant Pathogens (pp 131–142). CAB International, Wallingford.

    Google Scholar 

  • Bangera MG & Thomashow LS (1996) Characterization of a genomic locus required for synthesis of the antibiotic 2,4-diacetylphloroglucinol by the biological control agent Pseudomonas fluorescens Q2-87. Mol. Plant-Microbe Interact. 9: 83–90.

    PubMed  CAS  Google Scholar 

  • Bloemberg GV, O'Toole GA, Lugtenberg BJJ & Kolter R (1997) Green fluorescent protein as a marker for Pseudomonas spp. Appl. Environ. Microbiol. 63: 4543–4551.

    PubMed  CAS  Google Scholar 

  • Bloemberg GV, Wijfjes AHM, Lamers GEM, Stuurman N & Lugtenberg BJJ (2000) Simultaneous imaging of Pseudomonas fluorescensWCS365 populations expressing three different auto-fluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. Mol. Plant-Microbe Interact. 13: 1170–1176.

    PubMed  CAS  Google Scholar 

  • Bloemberg GV & Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Op. Plant Biol. 4: 343–350.

    Article  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. Proc. Natl. Acad. Sci. 96: 14073–14078.

    Article  PubMed  CAS  Google Scholar 

  • Bonas U, Ballvora A, Büttner D, Hahn K, Lahaye T, Marois E, Nennstiel D, Noel L, Pierre M, Szurek B, van den Ackerveken G & Rossier O (2000) Hrp type III secretion-mediated signaling between Xanthomonas and the plant. In: Wit de PJGM, Bisseling T, Stiekema WJ (Eds) Biology of Plant-Microbe Interactions (pp 23–28). International Society for Molecular Plant-Microbe Interactions, St. Paul, MN, USA.

    Google Scholar 

  • Bonfante P & Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytologist 130: 3–21.

    Article  Google Scholar 

  • Camacho MM (2000) Molecular characterization of type 4 pili, NDHI and PyrR in rhizosphere colonization of Pseudomonas fluorescens WCS365. Phd Thesis, Leiden University.

  • Chancey ST, Wood DW & Pierson III LS (1999) Two-component transcriptional regulation of N-acyl-homoserine lactone production in Pseudomonas aureofaciens. Appl. Environ. Microbiol. 65: 2294–2299.

    PubMed  CAS  Google Scholar 

  • Chin-A-Woeng TFC, Bloemberg GV, van der Bij AJ, van der Drift KMGM, Schripsema J, Kroon B, Scheffer RJ, Keel C, Bakker PAHM, Tichy H, de Bruijn FJ, Thomas-Oates JE & Lugtenberg BJJ (1998) Biocontrol by phenazine-1-carboxamide-producing Pseudomonas chlororaphis PCL1391 of tomato root rot caused by Fusarium oxysporum f. sp. radicis-lycopersici. Mol. Plant-Microbe Interact. 11: 1069–1077.

    CAS  Google Scholar 

  • Chin-A-Woeng TFC (2000) Molecular basis of biocontrol of tomato foot and root rot by Pseudomonas chlororaphis strain PCL1391. Phd Thesis, Leiden University.

  • Chin-A-Woeng TFC, Bloemberg GV, Mulders IHM, Dekkers LC & Lugtenberg BJJ (2000) Root colonization by Phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol. Plant-Microbe Interact. 13: 1340–1345.

    PubMed  CAS  Google Scholar 

  • Chin-A-Woeng TFC, van den Broek D, de Voer G, van der Drift KMGM, Tuinman S, Thomas-Oates JE, Lugtenberg BJJ & Bloemberg GV (2001) Phenazine-1-carboxamide production in the biocontrol strain Pseudomonas chlororaphis PCL1391 is regulated by multiple factors secreted into the growth medium. Mol. Plant-Microbe Interact. 14: 969–979.

    PubMed  CAS  Google Scholar 

  • Cornelis GR & Wolf-Watz H (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23: 861–867.

    Article  PubMed  CAS  Google Scholar 

  • Darzins A & Russell MA (1997) Molecular genetic analysis of type-4 pilus biogenesis and twitching motility using Pseudomonas aeruginosa as a model system-a review. Gene 192: 109–115.

    Article  PubMed  CAS  Google Scholar 

  • Dekkers LC, Phoelich CC, van der Fits L & Lugtenberg BJJ (1998) A site-specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365. Proc. Natl. Acad. Sci. 95: 7051–7056.

    Article  PubMed  CAS  Google Scholar 

  • Dekkers, LC, Mulders IHM, Phoelich CC, Chin-A-Woeng TFC, Wijfjes AHM & Lugtenberg BJJ (2000) The sss colonization gene of the tomato-Fusarium oxysporum f. sp. radicislycopersici biocontrol strain Pseudomonas fluorescens WCS365 can improve root colonization of other wild-type Pseudomonas spp. Bacteria. Mol. Plant-Microbe Interact. 13: 1177–1183.

    PubMed  CAS  Google Scholar 

  • Delaney I, Sheehan MM, 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. Microbiol. 146: 537–546.

    Google Scholar 

  • Delaney SM, Mavrodi DV, Bonsall RF & Thomashow LS (2001) phzO, a gene for biosynthesis of 2-hydroxylated phenazine com381 pounds in Pseudomonas aureofaciens 30-84. J. Bacteriol 183: 318–327.

    Article  PubMed  CAS  Google Scholar 

  • Déziel E, Comeau Y & Villemur R (2001) Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J. Bacteriol. 183: 1195–1204.

    Article  PubMed  Google Scholar 

  • Dörr J, Hurek T & Reinhold-Hurek B (1998) Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol. Microbiol. 30: 7–17.

    Article  PubMed  Google Scholar 

  • Duffy BK & Défago (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol. 65: 2429–2438.

    PubMed  CAS  Google Scholar 

  • Espinosa-Urgel M, Salido A & Ramos J-L (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J. Bacteriol. 182: 2363–2369.

    Article  PubMed  CAS  Google Scholar 

  • Felix G, Duran JD, Volko S & Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. The Plant Journal 18: 265–276.

    Article  PubMed  CAS  Google Scholar 

  • Flores M, Mavingui P, Perret X, Broughton WJ, Romero D, Hernández G, Dávila G & Palacios R (2000) Prediction, identification, and artificial selection of DNA rearrangements in Rhizobium: toward a natural genomic design. Proc. Natl. Acad. Sci. 97: 9138–9143.

    Article  PubMed  CAS  Google Scholar 

  • Fray RG, Throup JP, Daykin M, Wallace A, Williams P, Stewart GSAB & Grierson D (1999) Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nature Biotechnol. 17: 1017–1020.

    Article  CAS  Google Scholar 

  • Galán JE & Collmer A (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322–1328.

    Article  PubMed  Google Scholar 

  • Givskov M, Nys de R, Manefield M, Gram L, Masimillen R, Eberl L, Molin S, Steinberg PD & Kjelleberg S (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178: 6618–6622.

    PubMed  CAS  Google Scholar 

  • Goosen-de Roo L, de Maagd RA & Lugtenberg BJJ (1991) Antigenic changes in lipolysaccharide I of Rhizobium leguminosarum bv. viciae in root nodules of Vicia sativa subsp. nigra occur during release from injection threads. J. Bacteriol. 173: 3177–3183.

    PubMed  CAS  Google Scholar 

  • Haas D, Blumer C & Keel C (2000) Biocontrol ability of fluorescent pseudomonads genetically dissected: importance of positive feedback regulation. Curr. Opin. Biotech. 11: 290–297.

    Article  PubMed  CAS  Google Scholar 

  • Harrison MJ, Burleigh SH, Liu H & van Buuren ML (1996) Vesicular-Arbuscular mycorrhizae: molecular approaches to investigate phosphate nutrition in the symbiosis. In: Stacey G, Mullin B & Gresshoff PM (Eds) Biology of Plant-Microbe Interactions (pp 515–520) International Society for Molecular Plant-Microbe Interactions, St. Paul, MN, USA.

    Google Scholar 

  • He SY (1998) Type III protein secretion systems in plant and animal pathogenic bacteria. Annu. Rev. Phytopathol. 36: 363–392.

    Article  PubMed  CAS  Google Scholar 

  • Holden MTG, Chhabra SR, Nys de R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GPC, Stewart GSAB, Bycroft BW, Kjelleberg S & Williams P (1999) Quorum-sensing cross talk: Isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol. Microbiol. 33: 1254–1266.

    Article  PubMed  CAS  Google Scholar 

  • Hollingsworth RI & Carlson RW (1989) 27-Hydroxyoctacosanoic acid is a major structural fatty acyl component of the lipopolysaccharide of Rhizobium trifolii ANU 843. J. Biol. Chem. 264: 9300–9303.

    PubMed  CAS  Google Scholar 

  • Hutchinson ML, Gross D (1997) Lipopeptide phytotoxins produced by Pseudomonas syringae pv. syringae: comparison of the biosurfactant and ion channelforming activities of syringopeptin and syringomycin. Mol. Plant-Microbe Interact. 10: 347–354.

    Google Scholar 

  • Keel C, Wirthner PH, Oberhansli TH, Voisard C, Burger U, Haas D & Defago 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: 327–342.

    CAS  Google Scholar 

  • Keen NT (1996) Bacterial determinants of pathogenicity and avirulence - an overview. In: Stacey G, Mullin B & Gresshoff PM (Eds) Biology of Plant-Microbe Interactions (pp 145–152) International Society for Molecular Plant-Microbe Interactions, St. Paul, MN, USA.

    Google Scholar 

  • Kirner S, Hammer PE Hill DS, Altmann A, Fischer I, Weislo LJ, Lanahan M, van Pée K-H & Ligon JM (1998) Functions encoded by pyrrolnitrin biosynthetic genes from Pseudomonas fluorescens. J. Bacteriol. 180: 1939–1943.

    PubMed  CAS  Google Scholar 

  • Kjelleberg S, Steinberg P, Givskov M, Gram L, Manefield M & Nys de R (1997) Do marine natural products interfere with prokaryotic AHL regulatory systems? Aquat. Microb. Ecol. 13: 85–93.

    Google Scholar 

  • Kuiper I (2001) Molecular characterization of root colonizing Pseudomonas strains for rhizoremediation. PhD Thesis, Leiden University.

  • Kuiper I, Bloemberg GV & Lugtenberg BJJ (2001) Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol. Plant-Microbe Interact. 14: 1197–1205.

    PubMed  CAS  Google Scholar 

  • Lagopodi AL, Ram AFJ, Lamers GEM, Punt JP, Van den Hondel CAMJJ, Lugtenberg BJJ and Bloemberg GV (2002) Novel aspects of tomato root colonization and infection by Fusarium oxysporum F. sp. radicis-lycopersici revealed by confocal laser scanning microscopic analysis using the green fluorescent protein as a marker. Mol. Plant-Microbe Interact. 15: 172–179.

    PubMed  CAS  Google Scholar 

  • Lam E, Kato N & Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411: 848–853.

    Article  PubMed  CAS  Google Scholar 

  • Lee S-W & Cooksey DA (2000) Genes expressed in Pseudomonas putida during colonization of a plant-pathogenic fungus. Appl. Environ. Microbiol. 66: 2764–2772.

    Article  PubMed  CAS  Google Scholar 

  • Lindgren PB (1997) The role of hrp genes during plant-bacterial interactions. Annu. Rev. Phytopathol. 35: 129–152.

    Article  PubMed  CAS  Google Scholar 

  • Lindow SE (1995) Control of epiphytic ice nucleation-active bacteria for management of plant frost injury. In: Lee RE, Warren GJ & Gusta LV (Eds) Biological Ice Nucleation and its Applications (pp 239–256). American Phytopathological Society Press, St. Paul, MN, USA.

    Google Scholar 

  • Liyanage H, Palmer DA, Ulrich M & Bender CL (1995) Characterization and transcriptional analysis of the gene cluster for coronafacic acid, the polyketide component of the phytotoxin coronatine. Appl. Environ. Microbiol. 61: 3843–3848.

    PubMed  CAS  Google Scholar 

  • Lugtenberg BJJ (1998) Outer membrane proteins. In: Spaink HP, Kondorosi A & Hooykaas PJJ (Eds) The Rhizobiaceae (pp 45–53). Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Lugtenberg BJJ & Dekkers LC (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ. Microbiol. 1: 9–13.

    Article  PubMed  CAS  Google Scholar 

  • Lugtenberg BJJ, Dekkers L & Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39: 461–490.

    Article  PubMed  CAS  Google Scholar 

  • M'piga PM, Bélanger RR, Paulitz TC & Benhamou N (1997) Increased resistance to Fusarium oxysporum f. sp. radicislycopersici in tomato plants treated with the endophytic bacterium Pseudomonas fluorescens strain 63-28. Physiol. Mol. Plant Pathol. 50: 301–320.

    Article  Google Scholar 

  • Macnab RM (1999) The bacterial flagellum: reversible rotary propellor and type III export apparatus. J. Bacteriol. 181: 7149–7153.

    PubMed  CAS  Google Scholar 

  • Mahajan MS, Tan MW, Rahme LG & Ausubel FM (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa Caenorhabditis elegans pathogenesis model. Cell 96: 47–56.

    Article  Google Scholar 

  • Manefield M, Nys de R, Jumar N, Read R, Givskov M, Steinberg P & Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145: 283–291.

    Article  PubMed  CAS  Google Scholar 

  • Marie C, Broughton WJ & Deakin WJ (2001) Rhizobium type III secretion systems: legume charmers or alarmers? Curr. Op. Plant Biol. 4: 336–342.

    Article  CAS  Google Scholar 

  • Minder AC, Rudder KEE, Narberhaus F, Fischer H-M, Hennecke H & Geiger O (2001) Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Mol. Microbiol. 39: 1186–1198.

    Article  PubMed  CAS  Google Scholar 

  • Natera SHA, Guerreiro N & Djordjevic MA (2000) Proteome analysis of differentially displayed proteins as a tool for the investigation of symbiosis. Mol. Plant-Microbe Interact. 13: 995–1009.

    PubMed  CAS  Google Scholar 

  • Nielsen TH, Thrane C, Christophersen C, Anthoni U & Sørensen J (2000) Structure, production characteristics and fungal antagonism of tensin - a new antifungal cyclic lipopeptide from Pseudomonas fluorescens strain 96.578. J. Appl. Microbiol. 89: 992–1001.

    Article  PubMed  CAS  Google Scholar 

  • Nowak-Thompson, B, Chaney N, Wing JS, Gould SJ & Loper JE (1999) Characterization of the pyoluteorin biosynthetic gene cluster of Pseudomonas fluorescens Pf-5. J. Bacteriol. 181: 2166–2174.

    PubMed  CAS  Google Scholar 

  • O'Toole GA & Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295–304.

    Article  PubMed  Google Scholar 

  • Okinaka Y, Yang C-H, Ruiz MG & Keen NT (2001) Microarray profiling of gene expression in Erwinia chrysanthemi 3937 during plant infection. Abstract of 10th International Congr. on Mol. Plant-Microbe Interact. (Abstract #263).

  • Okon Y, Bloemberg GV & Lugtenberg BJJ (1998) Biotechnology of biofertilization and phytostimulation. In: Altman A (Ed) Agricultural Biotechnology (pp 327–349). Marcel Dekker Inc., New York.

    Google Scholar 

  • Ordentlich A, Elad Y & Chet I (1987) Rhizosphere colonization by Serratia marcescens for the control of Sclerotium RolfsII. Soil. Bio. Biochem. 19: 747–751.

    Article  Google Scholar 

  • Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS, Greenberg EP & Iglewski BH (1999) Quinolone signaling in the cell-tocell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. 96: 11229–11234.

    Article  PubMed  CAS  Google Scholar 

  • Pierson III LS, Keppenne VD & Wood DW (1994) Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30-84 is regulated by PhzR in response to cell density. J. Bacteriol. 176: 3966–3974.

    PubMed  CAS  Google Scholar 

  • Pierson LS, Gaffney T, Lam S & Gong F (1995) Molecular analysis of genes encoding phenazine biosynthesis in the biological control bacterium Pseudomonas aureofaciens. FEMS Microbiol. Lett. 134: 299–307.

    PubMed  CAS  Google Scholar 

  • Plessl J, Dorr J, Hurek T & Reinhold-Hurek B (2000) Interactions of Azoarcus spp. with rice: role of type 4 pili. Fourth European Nitrogen Fixation Conference. Sevilla, Spain. Abstract book, p. 31.

  • Poplawski AR, Chun W, Slater H, Daniels MJ & Dow M (1998) Synthesis of extracellular polysaccharide, extracellular enzymes and xanthomonadin in Xanthomonas campestris: Evidence for the involvement of two intercellular regulatory signals. Mol. Plant-Microbe Interact. 11: 68–70.

    Google Scholar 

  • Preston GM, Bertrand N, Jackson RW & Rainey PB (2001) Type III secretion in Pseudomonas fluorescens SBW25. Abstract of 10th International Congr. on Mol. Plant-Microbe Interact. (Abstract #671).

  • Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG & Ausubel FM (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899–1902.

    PubMed  CAS  Google Scholar 

  • Rainey PB (1999) Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 3: 243–257.

    Article  Google Scholar 

  • Reinhold-Hurek B & Hurek T (1998) Life in grasses: diazotrophic endophytes. Trends in Microbiol. 6: 139–144.

    Article  CAS  Google Scholar 

  • Romantschuk M & Bamford DH (1986) The causal agent of halo blight in bean, Pseudomonas syringae pv. phaseolicola, attaches to stomata via its pili. Microb. Pathog. 1: 139–148.

    Article  PubMed  CAS  Google Scholar 

  • Ronson C, Sullivan J, Trzebiatowski J, Gouzy J & de Bruijn F (2001) Comparative genomics of the symbiosis island of Mesorhizobium loti. In: Abstract of 10th International Congr. on Mol. Plant-Microbe Interact. (Abstract #66).

  • Ruiz-Lozano JM & Bonfante P (2000) A Burkholderia strain living inside the arbuscular mycorrhizal fungus Gigaspora margarita possesses the vacB gene, which is involved in host cell colonization by bacteria. Microb. Ecol. 39: 137–144.

    Article  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. J. Bacteriol. 182: 1215–1225.

    Article  PubMed  CAS  Google Scholar 

  • Schripsema J, de Rudder KEE, van Vliet TB, Lankhorst PP, de Vroom E, Kijne JW & van Brussel AAN (1996) Bacteriocin small of Rhizobium leguminosarum belongs to the class of N-acyl-l-homoserine lactone molecules, known as autoinducers and as quorum sensing co-transcription factors. J. Bacteriol. 178: 366–371.

    PubMed  CAS  Google Scholar 

  • Simon HM, Smith KP, Dodsworth JA, Guenthner B, Handelsman J & Goodman RM (2001) Influence of tomato genotype on growth of inoculated and indigenous bacteria in the spermosphere. Appl. Environ. Microbiol. 67: 514–520.

    Article  PubMed  CAS  Google Scholar 

  • Sivan A & Chet I (1989) The possible role of competition between Trichoderma harzianum and Fusarium oxysporum on rhizosphere colonization. Phytopathology 79: 198–203.

    Google Scholar 

  • Smith KP, Handelsman J & Goodman RM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc. Natl. Acad. Sci. 96: 4786–4790.

    Article  PubMed  CAS  Google Scholar 

  • Smith LM, Tola E, de Boer P & O'Gara F (1999) Signalling by the fungus Pythium ultimum represses expression of two ribosomal RNA operons with key roles in the rhizosphere ecology of Pseudomonas fluorescens F113. Environ. Microbiol. 6: 495–502.

    Article  Google Scholar 

  • Smith SE & Gianinazzi-Pearson V (1988) Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 39: 221–244.

    Article  CAS  Google Scholar 

  • Sohlenkamp C, Rudder KEE, Röhrs, V, López Lara IM & Geiger O (2000) Cloning and characterization of the gene for phosphatidylcholine synthase. J. Biol. Chem. 275: 18919–18925.

    Article  PubMed  CAS  Google Scholar 

  • Spaink HP, Kondorosi A & Hooykaas PJJ (Eds) (1998) In: The Rhizobiaceae: Molecular Biology of Model Plant-Associate Bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Ann. Rev. Microbiol. 54: 257–288.

    Article  CAS  Google Scholar 

  • Spaink HP, Bladergroen MR, Badelt K, Stronk OP & Schlaman WRM (2001) Avirulence factors from symbiotic bacteria. In: Abstract of 10th International Congr. on Mol. Plant-Microbe Interact. (Abstract #12).

  • Spellig T, Bottin A & Kahmann R (1996) Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252: 503–509.

    PubMed  CAS  Google Scholar 

  • Stanghellini ME & Miller RM (1997) Biosurfactants: Their identity and potential efficacy in the biological control of zoosporic plant pathogens. Plant Disease 81: 4–12.

    CAS  Google Scholar 

  • Steenhoudt O & Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev. 24: 487–506.

    Article  PubMed  CAS  Google Scholar 

  • Stohl EH, Stabb EV & Handelsman J (1996) Zwittermicin A and Biological control of Oomycete pathogens. In: Stacey G, Mullin B & Gresshoff PM (Eds) Biology of Plant-Microbe Interactions (pp 475–486). International Society forMolecular Plant-Microbe Interactions, St. Paul, MN, USA.

    Google Scholar 

  • Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ & Lagrou M et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959–964.

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M, Robinson JB & Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol. Plant-Microbe Interact. 13: 637–648.

    PubMed  CAS  Google Scholar 

  • Thomashow LS & Weller DM (1988) Role of phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritice. J. Bacteriol. 170: 3499–3508.

    PubMed  CAS  Google Scholar 

  • Thrane C, Nielsen TH, Nielsen MN, Sørensen J & Olsson S (2000) Viscosinamide-producing Pseudomonas fluorescens DR 54 exerts a biocontrol effect on Pythium ultimum in sugar beet rhizosphere. FEMS Microbiol. Ecol. 33: 139–146.

    Article  PubMed  CAS  Google Scholar 

  • Tombolini R, van der Gaag DJ, Gerhardson B & Jansson JK (1999) Colonization pattern of the biocontrol strain Pseudomonas chlororaphis MA 342 on Barley seeds visualized by using green fluorescent protein. Appl. Environ. Microbiol. 65: 3674–3680.

    PubMed  CAS  Google Scholar 

  • Vande Broek A, Lambrecht M, Eggermont K & Vanderleyden J (1999) Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. J. Bacteriol. 181: 1338–1342.

    PubMed  CAS  Google Scholar 

  • Van Loon LC, Bakker PAHM & Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36: 453–483.

    Article  PubMed  CAS  Google Scholar 

  • Van Peer R, Niemann GJ & Schippers B (1999) Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81: 728–734.

    Google Scholar 

  • Van Wees SCM, Swart de EAM, van Pelt JA, van Loon LC & Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate-and jasmonatedependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. 97: 8711–8716.

    Article  PubMed  CAS  Google Scholar 

  • Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CMT, Regensburg-Tuïnk TJG & Hooykaas PJJ (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290: 979–982.

    Article  PubMed  CAS  Google Scholar 

  • Viprey V, Del Greco A, Golinowski W, Broughton WJ & Perret X (1998) Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28: 1381–1389.

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Knill E, Glick BR & Défago G (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHAO and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can. J. Microbiol. 46: 898–907.

    Article  PubMed  CAS  Google Scholar 

  • Whistler CA, Stockwell VO & Loper JE (2000) Lon protease influences antibiotic production and UV tolerance of Pseudomonas fluorescens Pf-5. Appl. Environ. Microbiol. 66: 2718–2725.

    Article  PubMed  CAS  Google Scholar 

  • Whiteley M, Lee KM & Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. 96: 13904–13909.

    Article  PubMed  CAS  Google Scholar 

  • Wood DW, Chen L, Chen Y, Monks DE, Raymond C, Bovee D, Clendenning J, Kutyavin T, Zhou Y, Setubal JC, Okura VK, Kitajima JPW, Dolan M, Tomb JF, Zhang S, Kaul R, Olson MV, Gordon MP & Nester EW (2001) Sequencing and analysis of the Agrobacterium tumefaciensgenome. Abstract of 10th International Congr. on Mol. Plant-Microbe Interact. (Abstract #284).

  • Young GM, Schmiel DH & Miller VL (1999) A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl. Acad. Sci 96: 6456–6461.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Molecular Plant Sciences, Clusius Laboratory, Leiden University, Wassenaarseweg 64, 2333 AL, Leiden, The Netherlands

    Ben J.J. Lugtenberg, Thomas F.C. Chin-A-Woeng & Guido V. Bloemberg

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  1. Ben J.J. Lugtenberg
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  2. Thomas F.C. Chin-A-Woeng
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  3. Guido V. Bloemberg
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Lugtenberg, B.J., Chin-A-Woeng, T.F. & Bloemberg, G.V. Microbe–plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81, 373–383 (2002). https://doi.org/10.1023/A:1020596903142

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