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Antibiotic production by bacterial biocontrol agents

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Abstract

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.

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References

  • Akkermans ADL, Van Elsas JD & de Bruijn FJ (1995) Molecular Microbial Ecology Manual. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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: 3155–3166

    PubMed  CAS  Google Scholar 

  • Bender CL, Rangaswamy V & Loper JE (1999) Polyketide production by plant-associated pseudomonads. Annu. Rev. Phytopathol. 37: 175–196.

    Article  PubMed  CAS  Google Scholar 

  • Berg G (2000) Diversity of antifungal and plant-associated Serratia plymuthica strains. J. Appl. Microbiol. 88: 952–960.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  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, The Netherlands.

    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, 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 

  • Cook RJ (1993) Making greater use of introduced microorganisms for biological control of plant pathogens. Annu. Rev. Phytopathol. 31: 53–80.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Dorschel C (1997) The role of particle-beam LC-MS in separation development. LC-GC 15: 950–959.

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ellis RJ, Timms-Wilson TM, Bailey MJ (2000) Identification of conserved traits in fluorescent pseudomonads with antifungal activity. Environ. Microbiol. 2: 274–284.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Fravel DR (1988) Role of antibiosis in the biocontrol of plant diseases. Annu. Rev. Phytopathol. 26: 75–91.

    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. Nat. Biotech. 7: 1017–1020.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Gotlieb D (1976) The production and role of antibiotics in soil. J. Antibiot. 29: 987–1000.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Hammer PE, Hill S & Ligon J (1995) Characterization of genes from Pseudomonas fluorescens involved in the synthesis of pyrrolnitrin. Phytopathology 85: 1162.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Handelsman J & Stabb EV (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8: 1855–1869.

    Article  PubMed  CAS  Google Scholar 

  • Heungens K & Parke JL (2001) Postinfection biological control of oomycete pathogens of pea by Burkholderia cepacia AMMDR1. Phytopathology 91: 383–391.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Hoitink HAJ & Boehm MJ (1999) Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annu. Rev. Phytopathology 37: 427–446.

    Article  CAS  Google Scholar 

  • 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.

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Kerr A (1980) Biological control of crown gall through production of agrocin 84. Plant Dis. 64: 25–30.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Kloepper JW, Leong J, Teintze M & Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease suppressive soils. Curr. Microbiol. 4: 317–320.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Lindow SE (1995) The use of reporter genes in the study of microbial ecology. Mol. Ecol. 4: 555–566.

    CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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: 2541–2548

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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: 4334–4339

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Nishida M, Matsubara T & Watanabe N (1965) Pyrrolnitrin, a new antifungal antibiotic. Microbiological and toxicological observations. J. Antibiot. 18: 211–219.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    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 30-84. FEMS Microbiol. Lett. 134: 299–307.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Raaijmakers JM, Weller DM & Thomashow LS (1997) Frequency of antibiotic producing Pseudomonas spp. in natural environments. Appl. Environ. Microbiol. 63: 881–887.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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: 2023–2030

    PubMed  CAS  Google Scholar 

  • Silo-Suh LA, Stabb EV, Raffel SJ & Handelsman J (1998) Target range of Zwittermicin A, an aminopolyol antibiotic from Bacillus cereus. Curr. Micobiol 37: 6–11

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Stabb EV, Jacobson LM & Handelsman J (1994) Zwittermycin A-producing strains of Bacillus cereus from diverse soils. Appl. Environ. Microbiol. 60: 4404–4412.

    PubMed  CAS  Google Scholar 

  • Stohl EA, Milner JL & Handelsman J (1999) Zwittermicin A biosynthetic cluster. Gene 237: 403–411.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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: 1293–1300

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Van Elsas JD & Heijnen CE (1990) Methods for the introduction of bacteria into soil - a review. Biol. Fertil. Soils 10: 127–133.

    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 

  • 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.

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu. Rev. Phytopathol. 26: 379–407.

    Article  Google Scholar 

  • Whipps JM(1997) Developments in the biological control of soilborne plant pathogens. Adv. Bot. Res. 26: 1–133.

    Article  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52: 487–511.

    PubMed  CAS  Google Scholar 

  • Williams ST & Vickers JC (1986) The ecology of antibiotic production. Microb. Ecol. 12: 43–52.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Plant Sciences, Laboratory of Phytopathology, Wageningen University, Binnenhaven 5, 6709 PG, Wageningen, The Netherlands

    Jos M. Raaijmakers, Maria Vlami & Jorge T. de Souza

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  1. Jos M. Raaijmakers
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Raaijmakers, J.M., Vlami, M. & de Souza, J.T. Antibiotic production by bacterial biocontrol agents. Antonie Van Leeuwenhoek 81, 537–547 (2002). https://doi.org/10.1023/A:1020501420831

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