Antonie van Leeuwenhoek

, 81:537 | Cite as

Antibiotic production by bacterial biocontrol agents

  • Jos M. Raaijmakers
  • Maria Vlami
  • Jorge T. de Souza


Interest in biological control of plant pathogens has been stimulated in recent years by trends in agriculture towards greater sustainability and public concern about the use of hazardous pesticides. There is now unequivocal evidence that antibiotics play a key role in the suppression of various soilborne plant pathogens by antagonistic microorganisms. The significance of antibiotics in biocontrol, and more generally in microbial interactions, often has been questioned because of the indirect nature of the supporting evidence and the perceived constraints to antibiotic production in rhizosphere environments. Reporter gene systems and bio-analytical techniques have clearly demonstrated that antibiotics are produced in the spermosphere and rhizosphere of a variety of host plants. Several abiotic factors such as oxygen, temperature, specific carbon and nitrogen sources, and microelements have been identified to influence antibiotic production by bacteria biocontrol agents. Among the biotic factors that may play a determinative role in antibiotic production are the plant host, the pathogen, the indigenous microflora, and the cell density of the producing strain. This review presents recent advances in our understanding of antibiotic production by bacterial biocontrol agents and their role in microbial interactions.


Biological Control Biocontrol Agent Bacillus Cereus Antagonistic Bacterium Pyrrolnitrin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Akkermans ADL, Van Elsas JD & de Bruijn FJ (1995) Molecular Microbial Ecology Manual. Kluwer Academic Publishers, Dordrecht.Google Scholar
  2. Anjaiah V, Koedam N, Nowak-Thompson B, Loper JE, Hofte M, Tambong JT & Cornelis P (1998) Involvement of phenazines and anthranilate in the antagonism of Pseudomonas aeruginosa PNA1 and Tn 5 derivatives toward Fusarium spp. and Pythium spp. Mol. Plant-Microbe Interact. 11: 847–854.Google Scholar
  3. Bangera MG & Thomashow LS (1999) Identification and characterization of a gene cluster for synthesis of the polyketide antibiotic 2,4-diacetylphloroglucinol from Pseudomonas fluorescens Q2-87. J. Bacteriol. 181: 3155–3166PubMedGoogle Scholar
  4. Bender CL, Rangaswamy V & Loper JE (1999) Polyketide production by plant-associated pseudomonads. Annu. Rev. Phytopathol. 37: 175–196.PubMedCrossRefGoogle Scholar
  5. Berg G (2000) Diversity of antifungal and plant-associated Serratia plymuthica strains. J. Appl. Microbiol. 88: 952–960.PubMedCrossRefGoogle Scholar
  6. Bevivino A, Sarrocco S, Dalmastri C, Tabacchioni S, Cantale C, Chiarini L (1998) Characterization of a free-living maizerhizosphere population of Burkholderia cepacia: effect of seed treatment on disease suppression and growth promotion of maize. FEMS Microbiol. Ecol. 27: 225–237.CrossRefGoogle Scholar
  7. Bloemberg GV, Wijfjes AHM, Lamers GEM, Stuurman N & Lugtenberg BJJ (2000) Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different auto-fluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. Mol. Plant-Microbe Interact. 13: 1170–1176.PubMedGoogle Scholar
  8. Broderick NA, Goodman RM, Raffa KF & Handelsman J (2000) Synergy between zwittermicin A and Bacillus thuringiensis subsp kurstaki against gypsy moth (Lepidoptera:Lymantriidae). Environ. Entomol. 29: 101–107.CrossRefGoogle Scholar
  9. Burkhead KD, Schisler DA & Slininger PJ (1994) Pyrrolnitrin production by biological-control agent Pseudomonas cepacia B37w in culture and in colonized wounds of potatoes. Appl. Environ. Microbiol. 60: 2031–2039.PubMedGoogle Scholar
  10. Chernin L, Brandis A, Ismailov Z & Chet I (1996) Pyrrolnitrin production by an Enterobacter agglomerans strain with broad spectrum activity towards fungal and bacterial phytopathogens. Curr. Microbiol. 32: 208–212.CrossRefGoogle Scholar
  11. Chen F, Binder B & Hodson RE (2000) Flow cytometric detection of specific gene expression in prokaryotic cells using in situ RTPCR. FEMS Microbiol. Lett. 184: 291–295.PubMedCrossRefGoogle Scholar
  12. Chin-A-Woeng TFC (2000). Molecular basis of biocontrol of tomato foot and root rot by Pseudomonas chlororaphis strain PCL1391. PhD thesis, Leiden University, The Netherlands.Google Scholar
  13. Chin-A-Woeng TFC, Bloemberg GV, Van der Bij AJ, Van der Drift KMGM, Schripsema J, Kroon B, Scheffer RJ, Keel C, Bakker PAHM, 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. 10: 79–86.Google Scholar
  14. Cook RJ (1993) Making greater use of introduced microorganisms for biological control of plant pathogens. Annu. Rev. Phytopathol. 31: 53–80.CrossRefPubMedGoogle Scholar
  15. Cronin D, MoenneLoccoz Y, Fenton A, Dunne C, Dowling DN & OGara F (1997) Role of 2,4-diacetylphloroglucinol in the interactions of the biocontrol pseudomonad strain F113 with the potato cyst nematode Globodera rostochiensis. Appl. Environ. Microbiol. 63: 1357–1361.PubMedGoogle Scholar
  16. Delaney SM, Mavrodi DV, Bonsall RF & Thomashow LS (2001) PhzO, a gene for biosynthesis of 2-hydrolyated phenazine compounds in Pseudomonas aureofaciens 30-84. J. Bacteriol. 183: 318–327.PubMedCrossRefGoogle Scholar
  17. DiCello F, Bevivino A, Chiarini L, Fani R, Paffetti D, Tabacchioni S & Dalmastri C (1997) Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl. Environ. Microbiol. 63: 4485–4493.Google Scholar
  18. Dorschel C (1997) The role of particle-beam LC-MS in separation development. LC-GC 15: 950–959.Google Scholar
  19. Duffy BK & Defago G (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl. Environ. Microbiol. 65: 2429–2438.PubMedGoogle Scholar
  20. El-Banna N, Winkelmann G (1998) Pyrrolnitrin from Burkholderia cepacia: antibiotic activity against fungi and novel activities against streptomycetes. J. Appl. Microbiol. 85: 69–78.PubMedCrossRefGoogle Scholar
  21. Ellis RJ, Timms-Wilson TM, Bailey MJ (2000) Identification of conserved traits in fluorescent pseudomonads with antifungal activity. Environ. Microbiol. 2: 274–284.PubMedCrossRefGoogle Scholar
  22. Fenton AM, Stephens PM, Crowley J, Ocallaghan 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. Appl. Environ. Microbiol. 58: 3873–3878.PubMedGoogle Scholar
  23. Fravel DR (1988) Role of antibiosis in the biocontrol of plant diseases. Annu. Rev. Phytopathol. 26: 75–91.Google Scholar
  24. 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. Nat. Biotech. 7: 1017–1020.CrossRefGoogle Scholar
  25. Gaffney TD, Lam ST, Ligon JM, Gates K, Frazelle A, Dimaio J, Hill S, Goodwin S, Torkewitz N, Allshouse AM, Kempf HJ & Becker JO (1994) Global regulation of expression of antifungal factors by a Pseudomonas ffluorescens biological control strain. Mol. Plant-Microbe Interact. 7: 455–463.PubMedGoogle Scholar
  26. Gamard P, Sauriol F, Benhamou N, Belanger RR & Paulitz TC (1997) Novel butyrolactones with antifungal activity produced by Pseudomonas aureofaciens strain 63-28. J. Antibiot. 50: 742–749.PubMedGoogle Scholar
  27. Georgakopoulos D, Hendson M, Panopoulos NJ & Schroth MN (1994) Cloning of a phenazine biosynthetic locus of Pseudomonas aureofaciens PGS12 and analysis of its expression in vitro with the ice nucleation reporter gene. Appl. Environ. Microbiol. 60: 2931–2938.PubMedGoogle Scholar
  28. Giacomodonato MN, Pettinari MJ, Souto GI, Mendez BS & Lopez NI (2001) A PCR-based method for the screening of bacterial strains with antifungal activity in suppressive soybean rhizosphere. World J. Microbiol. Biotech. 17: 51–55.CrossRefGoogle Scholar
  29. Gotlieb D (1976) The production and role of antibiotics in soil. J. Antibiot. 29: 987–1000.Google Scholar
  30. Gutterson NI, Layton TJ, Ziegle JS & Warren GJ (1986) Molecular cloning and genetic determinants for inhibition of fungal growth by a fluorescent pseudomonad. J. Bacteriol. 165: 696–703.PubMedGoogle Scholar
  31. Hammer PE, Hill S & Ligon J (1995) Characterization of genes from Pseudomonas fluorescens involved in the synthesis of pyrrolnitrin. Phytopathology 85: 1162.Google Scholar
  32. Hammer PE, Hill DS, Lam ST, Van Pee KH & Ligon JM (1997). Four genes from Pseudomonas fluorescens that encode the biosynthesis of pyrrolnitrin. Appl. Environ. Microbiol. 63: 2147–2154.PubMedGoogle Scholar
  33. Hammer PE, Burd W, Hill DS, Ligon JM & van Pee KH (1999) Conservation of the pyrrolnitrin biosynthetic gene cluster among six pyrrolnitrin-producing strains. FEMS Microbiol. Lett. 180: 39–44.PubMedCrossRefGoogle Scholar
  34. Handelsman J & Stabb EV (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8: 1855–1869.PubMedCrossRefGoogle Scholar
  35. Heungens K & Parke JL (2001) Postinfection biological control of oomycete pathogens of pea by Burkholderia cepacia AMMDR1. Phytopathology 91: 383–391.PubMedGoogle Scholar
  36. Hodson RE, Dustman WA, Garg RP & Moran MA (1995) In situ PCR for visualization of microscale distribution of specific genes and gene products in prokaryotic communities. Appl. Environ. Microbiol. 61: 4074–4082.PubMedGoogle Scholar
  37. Hoitink HAJ & Boehm MJ (1999) Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annu. Rev. Phytopathology 37: 427–446.CrossRefGoogle Scholar
  38. Hokeberg M. Wright SAI, Svensson M, Lundgren LN & Gerhardson B (1998) Mutants of Pseudomonas chlororaphis defective in the production of an antifungal metabolite express reduced biocontrol activity. Abstract Proceedings ICPP98, Edinburgh, Scotland.Google Scholar
  39. Howell CR & Stipanovic RD (1979) Control of Rhizoctonia solani on cotton seedlings with Pseudomonas fluorescens and with an antibiotic produced by the bacterium. Phytopathology 69: 480–482.Google Scholar
  40. Kalbe C, Marten P & Berg G (1996) Strains of the genus Serratia as beneficial rhizobacteria of oilseed rape with antifungal properties. Microbiol. Res. 151: 433–439.PubMedGoogle Scholar
  41. Kang YW, Carlson R, Tharpe W & Schell MA (1998) Characterization of genes involved in biosynthesis of a novel antibiotic from Burkholderia cepacia BC11 and their role in biological control of Rhizoctonia solani. Appl. Environ. Microbiol. 64: 3939–3947.PubMedGoogle Scholar
  42. Keel C, Wirthner P, Oberhansli T, Voisard C, Burger, 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: 327–341.Google Scholar
  43. Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger P, Wirthner P, Haas D & Défago G (1992) Suppression of root diseases of by Pseudomonas fluorescens CHA0: importance of the secondary metabolite 2,4-diacetylphloroglucinol. Mol. Plant-Microbe Interact. 5: 4–13.Google Scholar
  44. Keel C, Weller DM, Natsch A, Défago G, Cook RJ & Thomashow LS (1996) Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas strains from diverse geographic locations. Appl. Environ. Microbiol. 62: 552–563.PubMedGoogle Scholar
  45. Kerr A (1980) Biological control of crown gall through production of agrocin 84. Plant Dis. 64: 25–30.Google Scholar
  46. Kim KK, Kang JG, Moon SS & Kang KY (2000) Isolation and identification of antifungal N-butylbenzenesulphonamide produced by Pseudomonas sp AB2. J. Antibiotics 53: 131–136.Google Scholar
  47. Kloepper JW, Leong J, Teintze M & Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease suppressive soils. Curr. Microbiol. 4: 317–320.Google Scholar
  48. Kraus J & Loper JE (1995) Characterization of a genomic region required for production of the antibiotic pyoluteorin by the biological control agent Pseudomonas fluorescens Pf-5. Appl. Environ. Microbiol. 61: 849–854.PubMedGoogle Scholar
  49. Levy E, Gough FJ, Berlin KD, Guiana PW & Smith JT (1992) Inhibition of Septoria tritici and other phytopathogenic fungi and bacteria by Pseudomonas fluorescens and its antibiotics. Plant Pathol. 41: 335–341.Google Scholar
  50. Ligon JM, Hill DS, Hammer PE, Torkewitz NR, Hofmann D, Kempf HJ & van Pee KH (2000) Natural products with antifungal activity from Pseudomonas biocontrol bacteria. Pest Manage. Sci. 56: 688–695.CrossRefGoogle Scholar
  51. Lindow SE (1995) The use of reporter genes in the study of microbial ecology. Mol. Ecol. 4: 555–566.Google Scholar
  52. Loper JE & Lindow SE (1997) Reporter gene systems useful in evaluating gene expression by soil-and plant-associated bacteria. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenbach LD & Walter MV (Eds) Manual of Environmental Microbiology. (pp 482–492) ASM Press, Washington, DC.Google Scholar
  53. Maurhofer M, Keel C, Schnider U, Voisard C, Haas D & Defago G (1992) Influence of enhanced antibiotic production in Pseudomonas fluorescens strain CHA0 on its disease suppressive capacity. Phytopathology 82: 190–195.Google Scholar
  54. Mavrodi DV, Ksenzenko VN, Bonsall RF, Cook RJ, Boronin AM & Thomashow LS (1998) A seven-gene locus for synthesis of phenazine-1-carboxylic acid by Pseudomonas fluorescens 2-79. J. Bacteriol. 180: 2541–2548PubMedGoogle Scholar
  55. McSpadden-Gardener BB, Schroeder KL, Kalloger SE, Raaijmakers JM, Thomashow LS & Weller DM (2000) Genotypic and phenotypic diversity of phlD-containing Pseudomonas isolated from the rhizosphere of wheat. Appl. Environ. Microbiol. 66: 1939–1946.PubMedCrossRefGoogle Scholar
  56. Milner JL, Silo-Suh L, Lee JC, He HY, Clardy J & Handelsman J (1996) Production of kanosamine by Bacillus cereus UW85. Appl Environ. Microbiol. 62: 3061–3065.PubMedGoogle Scholar
  57. Nakayama T, Homma Y, Hashidoko Y, Mizutani J & Tahara S (1999) Possible role of xanthobaccins produced by Stenotrophomonas sp strain SB-K88 in suppression of sugar beet damping-off disease. Appl. Environ. Microbiol. 55: 4334–4339Google Scholar
  58. Nielsen MN, Sorensen J, Fels J & Pedersen HC (1998) Secondary metabolite-and endochitinase-dependent antagonism toward plant-pathogenic microfungi of Pseudomonas fluorescens isolates from sugar beet rhizosphere. Appl. Environ. Microbiol. 64: 3563–3569.PubMedGoogle Scholar
  59. Nishida M, Matsubara T & Watanabe N (1965) Pyrrolnitrin, a new antifungal antibiotic. Microbiological and toxicological observations. J. Antibiot. 18: 211–219.PubMedGoogle Scholar
  60. Nowak-Thompson B, Chaney N, Wing JS, Gould SJ and Loper JE (1999). Characterization of the pyoluteorin biosynthetic gene cluster of Pseudomonas fluorescens Pf-5. J. Bacteriol 181: 2166–2174.PubMedGoogle Scholar
  61. Ownley BH, Weller DM & Thomashow LS (1992) Influence of in situ and in vitro pH on suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens 2-79. Phytopathology 82: 178–184.Google Scholar
  62. Parke JL & Gurian-Sherman D (2001) Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu. Rev. Phytopathol. 39: 225–258.PubMedCrossRefGoogle Scholar
  63. Paulitz T, Nowak-Thompson B, Gamard P, Tsang E & Loper JE (2000) A novel antifungal furanone from Pseudomonas aureofaciens, a biocontrol agent of fungal plant pathogens. J. Chem. Ecol. 26: 1515–1524.CrossRefGoogle Scholar
  64. Picard C, di Cello F, Ventura M, Fani R & Guckert A (2000) Frequency and diversity of 2,4-diacetylphloroglucinol-producing bacteria isolated from the maize rhizosphere at different stages of growth. Appl. Environ. Microbiol. 66: 948–955.PubMedCrossRefGoogle Scholar
  65. Pierson LS & Thomashow LS (1992) Cloning and heterologous expression of the phenazine biosynthetic locus from Pseudomonas aureofaciens 30-84. Mol. Plant-Microbe Interact. 5: 330–339.PubMedGoogle Scholar
  66. Pierson LS, Gaffney T, Lam S & Gong F (1995) Molecular analysis of genes encoding phenazine biosynthesis in the biological control bacterium Pseudomonas aureofaciens 30-84. FEMS Microbiol. Lett. 134: 299–307.PubMedGoogle Scholar
  67. Raaijmakers JM & Weller DM (1998) Natural plant protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol. Plant-Microbe Interact. 11: 144–152.Google Scholar
  68. Raaijmakers JM, Weller DM & Thomashow LS (1997) Frequency of antibiotic producing Pseudomonas spp. in natural environments. Appl. Environ. Microbiol. 63: 881–887.PubMedGoogle Scholar
  69. Raaijmakers JM, Bonsall RF & Weller DM (1999) Effect of population density of Pseudomonas fluorescens on production of 2,4-diacetylphloroglucinol in the rhizosphere of wheat. Phytopathology 89: 470–475.PubMedGoogle Scholar
  70. Raaijmakers JM & Weller DM (2001) Exploiting genotypic diversity of 2,4-diacetylphloroglucinol-producing Pseudomonas spp.: characterization of superior root-colonizing P. fluorescens strain Q8r1-96. Appl. Environ. Microbiol. 67: 2545–2554.PubMedCrossRefGoogle Scholar
  71. Raffel SJ, Stabb EV, Milner JL & Handelsman J (1996) Genotypic and phenotypic analysis of zwittermicin A-producing strains of Bacillus cereus. Microbiology 142: 3425–3436.PubMedCrossRefGoogle Scholar
  72. Rosales AM, Thomashow LS, Cook RJ & Mew TW (1995) Isolation and identification of antifungal metabolites produced by rice-associated antagonistic Pseudomonas spp. Phytopathology 85: 1028–1032.Google Scholar
  73. Sarniguet A, Kraus J, Henkels MD, Muehlchen AM & Loper JE (1995) The sigma factor sigma(S) affects antibiotic production and biological control activity of Pseudomonas fluorescens Pf-5. Proc. Natl. Acad. Sci. USA 92: 12255–12259.PubMedCrossRefGoogle Scholar
  74. Shanahan P, O'Sullivan DJ, Simpson P, Glennon JD & O'Gara F (1992) Isolation of 2,4-diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing its production. Appl. Environ. Microbiol. 58: 353–358.PubMedGoogle Scholar
  75. Sharifi-Tehrani A, Zala M, Natsch A, Moënne-Loccoz Y & Défago G (1998) Biocontrol of soil-borne fungal plant diseases by 2-4-diacetylphloroglucinol-producing fluorescent pseudomonads with different restriction profiles of amplified 16S rDNA. Eur. J. Plant Pathol. 104: 631–643.CrossRefGoogle Scholar
  76. Silo-Suh LA, Lethbridge BJ, Raffel SI, He HY, Clardy J & Handelsman J (1994) Biological-activities of 2 fungistatic antibiotics produced by Bacillus cereus UW85. Appl. Environ. Microbiol. 60: 2023–2030PubMedGoogle Scholar
  77. Silo-Suh LA, Stabb EV, Raffel SJ & Handelsman J (1998) Target range of Zwittermicin A, an aminopolyol antibiotic from Bacillus cereus. Curr. Micobiol 37: 6–11CrossRefGoogle Scholar
  78. Slininger PJ & Jackson MA (1992) Nutrtional factors regulating growth and accumulation of phenazine-1-carboxylic acid by Pseudomonas fluorescens 2-79. Appl.Microbiol. Biotechnol. 37: 388–392.CrossRefGoogle Scholar
  79. Smith KP, Handelsman J & Goodman RM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc. Nat. Ac. Sciences USA 96: 4786–4790.CrossRefGoogle Scholar
  80. Stabb EV, Jacobson LM & Handelsman J (1994) Zwittermycin A-producing strains of Bacillus cereus from diverse soils. Appl. Environ. Microbiol. 60: 4404–4412.PubMedGoogle Scholar
  81. Stohl EA, Milner JL & Handelsman J (1999) Zwittermicin A biosynthetic cluster. Gene 237: 403–411.PubMedCrossRefGoogle Scholar
  82. Thomashow LS & Weller DM (1988) Role of phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J. Bacteriol. 170: 3499–3508.PubMedGoogle Scholar
  83. Thomashow LS & Weller DM (1996) Current concepts in the use of introduced bacteria for biological disease control: mechanisms and antifungal metabolites. In: Stacey G & Keen NT (Eds), Plant-Microbe Interactions, Vol. 1, (pp 187–236). Chapman & Hall, New York.Google Scholar
  84. Thomashow LS, Bonsall RF & Weller DM (1997) Antibiotic production by soil and rhizosphere microbes in situ. In: Hurst CJ, Knudsen GR, McInerney MJ, Stetzenbach LD & Walter MV (Eds) Manual of Environmental Microbiology, (pp 493–499). ASM Press, Washington, DC.Google Scholar
  85. Timms-Wilson TM, Ellis RJ, Renwick A, Rhodes DJ, Mavrodi DV, Weller DM, Thomashow LS & Bailey MJ (2000) Chromosomal insertion of phenazine-1-carboxylic acid biosynthetic pathway enhances efficacy of damping-off disease control by Pseudomonas fluorescens. Mol. Plant-Microbe Interact. 13: 1293–1300PubMedGoogle Scholar
  86. Trejo-Estrada SR, Paszczynski A & Crawford DL (1998) Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9. J. Industr. Microbiol. Biotech. 21: 81–90.CrossRefGoogle Scholar
  87. Van Elsas JD & Heijnen CE (1990) Methods for the introduction of bacteria into soil - a review. Biol. Fertil. Soils 10: 127–133.Google Scholar
  88. Van Loon LC, Bakker PAHM & Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36: 453–483PubMedCrossRefGoogle Scholar
  89. Vincent MN, Harrison LA, Brackin JM, Kovacevich PA, Murkerji P, Weller DM & Pierson EA (1991) Genetic analysis of the antifungal activity of a soilborne Pseudomonas aureofaciens strain. Appl. Environ. Microbiol. 57: 2928–2934.PubMedGoogle Scholar
  90. Weller DM (1983) Colonization of wheat roots by a fluorescent pseudomonad suppressive to take-all. Phytopathology 73: 1548–1553.CrossRefGoogle Scholar
  91. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26: 379–407.CrossRefGoogle Scholar
  92. Whipps JM(1997) Developments in the biological control of soilborne plant pathogens. Adv. Bot. Res. 26: 1–133.CrossRefGoogle Scholar
  93. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52: 487–511.PubMedGoogle Scholar
  94. Williams ST & Vickers JC (1986) The ecology of antibiotic production. Microb. Ecol. 12: 43–52.CrossRefGoogle Scholar
  95. Wood DW, Gong F, Daykin Mm, Williams P & Pierson LS (1997) N-Acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30-84 in the wheat rhizosphere. J. Bacteriol. 179: 7663–7670.PubMedGoogle Scholar
  96. Wright SAI, Zumoff CH, Schneider L & Beer SV (2001) Pantoea agglomerans strain EH318 produces two antibiotics that inhibit Erwinia amylovora in vitro. Appl. Environ. Microbiol. 67: 284–292.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Jos M. Raaijmakers
    • 1
  • Maria Vlami
    • 1
  • Jorge T. de Souza
    • 1
  1. 1.Department of Plant Sciences, Laboratory of PhytopathologyWageningen UniversityWageningenThe Netherlands

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