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Phenazine-Producing Pseudomonas spp. as Biocontrol Agents of Plant Pathogens

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Book cover Microbial Inoculants in Sustainable Agricultural Productivity

Abstract

Soils that are suppressive to diseases have often been shown to contain high levels of fluorescent Pseudomonas spp. that produce a variety of secondary metabolites, including antibiotics such as hydrogen cyanide, diacetylphloroglucinol (DAPG) and phenazines, among others. Phenazine-producing Pseudomonas spp. show promise for use as successful biocontrol agents against many diseases affecting several agricultural crops. The production of different types of phenazines (phenazine-1-carboxylic acid (PCA), phenazine-1-carboxamide (PCN), hydroxyphenazines (OH-PHZ) and pyocyanin (PYO)) has been shown to be directly involved in the reduction of several diseases caused by fungi, oomycetes and bacteria, in a variety of geographical locations. Phenazines can also be highly important in fluorescent Pseudomonas spp. physiology and have the potential to increase fitness of the producing strains by affecting traits such as biofilm formation and iron acquisition. The high capacity for soil colonization as well as the robustness and competitiveness of fluorescent Pseudomonas spp. show potential for their increased use in commercial applications. However, further studies are needed to determine the optimal conditions under which these bacteria can persist and produce phenazines under natural soil conditions, and their implication at the molecular, physiological, and ecological levels.

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References

  • Agusti L, Bonaterra A, Moragrega C, Camps J, Montesinos E (2011) Biocontrol of root rot of strawberry caused by Phytophthora cactorum with a combination of two Pseudomonas fluorescens strains. J Plant Pathol 93:363–372

    CAS  Google Scholar 

  • Ahuja EG, Janning P, Mentel M, Graebsch A, Breinbauer R, Hiller W, Costisella B, Thomashow LS, Mavrodi DV, Blankenfeldt W (2008) PhzA/B catalyzes the formation of the tricycle in phenazine biosynthesis. J Am Chem Soc 130:17053–17061

    Article  CAS  PubMed  Google Scholar 

  • Ali Siddiqui I, Ehetshamul-Haque S, Shahid Shaukat S (2001) Use of rhizobacteria in the control of root rot–root knot disease complex of mungbean. J Phytopathol 149:337–346

    Article  Google Scholar 

  • Anjaiah V, Koedam N, Nowak-Thompson B, Loper JE, Höfte 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

    Article  CAS  Google Scholar 

  • Arora NK, Khare E, Maheshwari DK (2011) Plant growth promoting rhizobacteria: constraints in bioformulation, commercialization and future strategies. In: Maheshwari DK (ed) Plant growth and health promoting bacteria. Springer, Berlin/Heidelberg, pp 97–116

    Google Scholar 

  • Arseneault T, Goyer C, Filion M (2013) Phenazine production by Pseudomonas sp. LBUM223 contributes to the biological control of potato common scab. Phytopathology 103:995–1000

    Article  CAS  PubMed  Google Scholar 

  • Arseneault T, Goyer C, Filion M (2015) Pseudomonas fluorescens LBUM223 increases potato yield and reduces common scab symptoms in the field. Phytopathology 105:1311-1317

    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. Mol Plant Microbe Interact 15:1147–1156

    Article  CAS  PubMed  Google Scholar 

  • Bankhead SB, Landa BB, Lutton E, Weller DM, McSpadden Gardener BB (2004) Minimal changes in rhizobacterial population structure following root colonization by wild type and transgenic biocontrol strains. FEMS Microbiol Ecol 49:307–318

    Article  CAS  PubMed  Google Scholar 

  • Baraquet C, Murakami K, Parsek MR, Harwood CS (2012) The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res 40:7207–7218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bardas GA, Lagopodi AL, Kadoglidou K, Tzavella-Klonari K (2009) Biological control of three Colletotrichum lindemuthianum races using Pseudomonas chlororaphis PCL1391 and Pseudomonas fluorescens WCS365. Biol Control 49:139–145

    Article  Google Scholar 

  • Baron S, Terranova G, Rowe J (1989) Molecular mechanism of the antimicrobial action of pyocyanin. Curr Microbiol 18:223–230

    Article  CAS  Google Scholar 

  • Blankenfeldt W (2013) The biosynthesis of phenazines. In: Chincholcar S, Thomashow LS (eds) Microbial phenazines: biosynthesis, agriculture and health. Springer, Berlin/Heidelberg, pp 1–17

    Chapter  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burr TJ, Schroth MN, Suslow T (1978) Increased potato yields by treatment of seedpieces with specific strains of Pseudomonas fluorescens and P. putida. Phytopathology 68:1377–1383

    Article  Google Scholar 

  • Chin-A-Woeng T, Bloemberg GV, van der Bij A, van der Drift K, Schripsema J, Kroon B, Scheffer R, Keel C, Bakker P, Tichy H-V, de Bruijn F, Thomas-Oates JE, Lugtenberg B (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

    Article  CAS  Google Scholar 

  • Chin-A-Woeng TFC, Bloemberg GV, Mulders IH, Dekkers LC, Lugtenberg BJ (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

    Article  CAS  PubMed  Google Scholar 

  • Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2003) Phenazines and their role in biocontrol by Pseudomonas bacteria. New Phytol 157:503–523

    Article  CAS  Google Scholar 

  • Couillerot O, Prigent-Combaret C, Caballero-Mellado J, Moënne-Loccoz Y (2009) Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Lett Appl Microbiol 48:505–512

    Article  CAS  PubMed  Google Scholar 

  • D’aes J, Hua GKH, De Maeyer K, Pannecoucque J, Forrez I, Ongena M, Dietrich LEP, Thomashow LS, Mavrodi DV, Höfte M (2011) Biological control of Rhizoctonia root rot on bean by phenazine- and cyclic lipopeptide-producing Pseudomonas CMR12a. Phytopathology 101:996–1004

    Article  PubMed  Google Scholar 

  • D’aes J, Kieu NP, Léclère V, Tokarski C, Olorunleke FE, De Maeyer K, Jacques P, Höfte M, Ongena M (2014) To settle or to move? The interplay between two classes of cyclic lipopeptides in the biocontrol strain Pseudomonas CMR12a. Environ Microbiol 16:2282–2300

    Article  PubMed  Google Scholar 

  • Das T, Kutty SK, Kumar N, Manefield M (2013) Pyocyanin facilitates extracellular DNA binding to Pseudomonas aeruginosa influencing cell surface properties and aggregation. PLoS One 8, e58299. doi:10.1371/journal.pone.0058299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies DG, Parsek M, Pearson J, Iglewski B, Costerton J, Greenberg E (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468

    Article  CAS  PubMed  Google Scholar 

  • Gamage S, Spicer J, Rewcastle G, Milton J, Sohal S, Dangerfield W, Mistry P, Vicker N, Charlton P, Denny W (2002) Structure-activity relationships for pyrido-, imidazo-, pyrazolo-, pyrazino-, and pyrrolophenazinecarboxamides as topoisomerase-targeted anticancer agents. J Med Chem 45:740–743

    Article  CAS  PubMed  Google Scholar 

  • Givskov M, Eberl L, Møller S, Poulsen LK, Molin S (1994) Responses to nutrient starvation in Pseudomonas putida KT2442: analysis of general cross-protection, cell shape, and macromolecular content. J Bacteriol 176:7–14

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319

    Article  CAS  PubMed  Google Scholar 

  • Harman GE, Obregón MA, Samuels GJ, Lorito M (2010) Changing models for commercialization and implementation of biocontrol in the developing and the developed world. Plant Dis 94:928–939

    Article  Google Scholar 

  • Hassan HM, Fridovich I (1980) Mechanism of the antibiotic action pyocyanine. J Bacteriol 141:156–163

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hernandez ME, Kappler A, Newman DK (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70:921–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu W, Gao Q, Hamada MS, Dawood DH, Zheng J, Chen Y, Ma Z (2014) Potential of Pseudomonas chlororaphis subsp. aurantiaca strain Pcho10 as a biocontrol agent against Fusarium graminearum. Phytopathology 104:1289–1297

    Article  CAS  PubMed  Google Scholar 

  • Jasim B, Anisha C, Rohini S, Kurian JM, Jyothis M, Radhakrishnan EK (2014) Phenazine carboxylic acid production and rhizome protective effect of endophytic Pseudomonas aeruginosa isolated from Zingiber officinale. World J Microbiol Biotechnol 30:1649–1654

    Article  CAS  PubMed  Google Scholar 

  • Jayaseelan S, Ramaswamy D, Dharmaraj S (2014) Pyocyanin: production, applications, challenges and new insights. World J Microbiol Biotechnol 30:1159–1168

    Article  CAS  PubMed  Google Scholar 

  • Johnsson L, Hökeberg M, Gerhardson B (1998) Performance of the Pseudomonas chlororaphis biocontrol agent MA 342 against cereal seed-borne diseases in field experiments. Eur J Plant Pathol 104:701–711

    Article  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khan SR, Herman J, Krank J, Serkova NJ, Churchill MEA, Suga H, Farrand SK (2007) N-(3-hydroxyhexanoyl)-L-homoserine lactone is the biologically relevant quormone that regulates the phz operon of Pseudomonas chlororaphis strain 30–84. Appl Environ Microbiol 73:7443–7455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khatri BB, Tegg RS, Brown PH, Wilson CR (2011) Temporal association of potato tuber development with susceptibility to common scab and Streptomyces scabiei-induced responses in the potato periderm. Plant Pathol 60:776–786

    Article  Google Scholar 

  • Kloepper JW, Schroth MN, Miller TD (1980) Effects of rhizosphere colonization by plant growth-promoting rhizobacteria on potato plant development and yield. Phytopathology 70:1078–1082

    Article  Google Scholar 

  • Latour X, Philippot L, Corberand T, Lemanceau P (1999) The establishment of an introduced community of fluorescent pseudomonads in the soil and in the rhizosphere is affected by the soil type. FEMS Microbiol Ecol 30:163–170

    Article  CAS  PubMed  Google Scholar 

  • Lau GW, Hassett DJ, Ran H, Kong F (2004) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10:599–606

    Article  CAS  PubMed  Google Scholar 

  • Lottmann J, Heuer H, de Vries J, Mahn A, Düring K, Wackernagel W, Smalla K, Berg G (2000) Establishment of introduced antagonistic bacteria in the rhizosphere of transgenic potatoes and their effect on the bacterial community. FEMS Microbiol Ecol 33:41–49

    Article  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  PubMed  Google Scholar 

  • Maddula VSRK, Zhang Z, Pierson EA, Pierson LS III (2006) Quorum sensing and phenazines are involved in biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30–84. Microb Ecol 52:289–301

    Article  CAS  PubMed  Google Scholar 

  • Maddula VSRK, Pierson EA, Pierson LS III (2008) Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30–84: effects on biofilm formation and pathogen inhibition. J Bacteriol 190:2759–2766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mark GL, Morrissey JP, Higgins P, O’Gara F (2006) Molecular-based strategies to exploit Pseudomonas biocontrol strains for environmental biotechnology applications. FEMS Microbiol Ecol 56:167–177

    Article  CAS  PubMed  Google Scholar 

  • Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G, Thomashow LS (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183:6454–6465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mavrodi DV, Blankenfeldt W, Thomashow LS (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44:417–445

    Article  CAS  PubMed  Google Scholar 

  • Mavrodi DV, Peever TL, Mavrodi OV, Parejko JA, Raaijmakers JM, Lemanceau P, Mazurier S, Heide L, Blankenfeldt W, Weller DM, Thomashow LS (2010) Diversity and evolution of the phenazine biosynthesis pathway. Appl Environ Microbiol 76:866–879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mavrodi DV, Mavrodi OV, Parejko JA, Bonsall RF, Kwak Y-S, Paulitz TC, Thomashow LS, Weller DM (2012a) Accumulation of the antibiotic phenazine-1-carboxylic acid in the rhizosphere of dryland cereals. Appl Environ Microbiol 78:804–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mavrodi OV, Mavrodi DV, Parejko JA, Thomashow LS, Weller DM (2012b) Irrigation differentially impacts populations of indigenous antibiotic-producing Pseudomonas spp. in the rhizosphere of wheat. Appl Environ Microbiol 78:3214–3220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mavrodi DV, Parejko JA, Mavrodi OV, Kwak Y-S, Weller DM, Blankenfeldt W, Thomashow LS (2013) Recent insights into the diversity, frequency and ecological roles of phenazines in fluorescent Pseudomonas spp. Environ Microbiol 15:675–686

    Article  CAS  PubMed  Google Scholar 

  • Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM (2009) Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J 3:977–991

    Article  CAS  PubMed  Google Scholar 

  • Mazzola M, Cook RJ, Thomashow LS, Weller DM, Pierson LS III (1992) Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent Pseudomonads in soil habitats. Appl Environ Microbiol 58:2616–2624

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mercado-Blanco J, Bakker PAHM (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 92:367–389

    Article  PubMed  Google Scholar 

  • O’Malley Y, Reszka K, Rasmussen G, Abdalla M, Denning G, Britigan B (2003) The Pseudomonas secretory product pyocyanin inhibits catalase activity in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol 285:L1077–L1086

    Article  PubMed  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

    Article  CAS  Google Scholar 

  • Ownley BH, Duffy BK, Weller DM (2003) Identification and manipulation of soil properties to improve the biological control performance of phenazine-producing Pseudomonas fluorescens. Appl Environ Microbiol 69:3333–3343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parejko JA, Mavrodi DV, Mavrodi OV, Weller DM, Thomashow LS (2012) Population structure and diversity of phenazine-1-carboxylic acid producing fluorescent Pseudomonas spp. from dryland cereal fields of central Washington State (USA). Microb Ecol 64:226–241

    Article  PubMed  Google Scholar 

  • Park JY, Oh SA, Anderson AJ, Neiswender J, Kim J-C, Kim YC (2011) Production of the antifungal compounds phenazine and pyrrolnitrin from Pseudomonas chlororaphis O6 is differentially regulated by glucose. Lett Appl Microbiol 52:532–537

    Article  CAS  PubMed  Google Scholar 

  • Perneel M, D’hondt L, De Maeyer K, Adiobo A, Rabaey K, Höfte M (2008) Phenazines and biosurfactants interact in the biological control of soil-borne diseases caused by Pythium spp. Environ Microbiol 10:778–788

    Article  PubMed  Google Scholar 

  • Pierson LS III, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pierson EA, Wood DW, Cannon JA, Blachere FM, Pierson LS III (1998) Interpopulation signaling via N-Acyl-Homoserine lactones among bacteria in the wheat rhizosphere. Mol Plant Microbe Interact 11:1078–1084

    Article  CAS  Google Scholar 

  • Pliego C, Ramos C, de Vicente A, Cazorla FM (2011) Screening for candidate bacterial biocontrol agents against soilborne fungal plant pathogens. Plant Soil 340:505–520

    Article  CAS  Google Scholar 

  • Powell J, Vargas J Jr, Nair M, Detweiler A, Chandra A (2000) Management of dollar spot on creeping bentgrass with metabolites of Pseudomonas aureofaciens (TX-1). Plant Dis 84:19–24

    Article  CAS  Google Scholar 

  • Price-Whelan A, Dietrich LEP, Newman DK (2006) Rethinking “secondary” metabolism: physiological roles for phenazine antibiotics. Nat Chem Biol 2:71–78

    Article  CAS  PubMed  Google Scholar 

  • Price-Whelan A, Dietrich LEP, Newman DK (2007) Pyocyanin alters redox homeostasis and carbon flux through central metabolic pathways in Pseudomonas aeruginosa PA14. J Bacteriol 189:6372–6381

    Article  CAS  PubMed  PubMed Central  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

    Article  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raio A, Puopolo G, Cimmino A, Danti R, Della Rocca G, Evidente A (2011) Biocontrol of cypress canker by the phenazine producer Pseudomonas chlororaphis subsp. aureofaciens strain M71. Biol Control 58:133–138

    Article  CAS  Google Scholar 

  • Ramey BE, Koutsoudis M, von Bodman SB, Fuqua C (2004) Biofilm formation in plant-microbe associations. Curr Opin Microbiol 7:602–609

    Article  CAS  PubMed  Google Scholar 

  • Ran H, Hassett DJ, Lau GW (2003) Human targets of Pseudomonas aeruginosa pyocyanin. Proc Natl Acad Sci U S A 100:14315–14320

    Article  CAS  PubMed  PubMed Central  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. J Bacteriol 187:276–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selin C, Habibian R, Poritsanos N, Athukorala SNP, Fernando D, de Kievit TR (2010) Phenazines are not essential for Pseudomonas chlororaphis PA23 biocontrol of Sclerotinia sclerotiorum, but do play a role in biofilm formation. FEMS Microbiol Ecol 71:73–83

    Article  CAS  PubMed  Google Scholar 

  • Sigler WV, Nakatsu CH, Reicher ZJ, Turco RF (2001) Fate of the biological control agent Pseudomonas aureofaciens TX-1 after application to turfgrass. Appl Environ Microbiol 67:3542–3548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slininger PJ, Shea-Wilbur MA (1995) Liquid-culture pH, temperature, and carbon (not nitrogen) source regulate phenazine productivity of the take-all biocontrol agent Pseudomonas fluorescens 2–79. Appl Microbiol Biotechnol 43:794–800

    Article  CAS  PubMed  Google Scholar 

  • Slininger PJ, Schisler DA, Shea-Andersh MA, Sloan JM, Woodell LK, Frazier MJ, Olsen NL (2010) Multi-strain co-cultures surpass blends for broad spectrum biological control of maladies of potatoes in storage. Biocontrol Sci Technol 20:763–786

    Article  Google Scholar 

  • Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. CRC Crit Rev Plant Sci 19:1–30

    Article  Google Scholar 

  • Sundh I, Goettel MS (2013) Regulating biocontrol agents: a historical perspective and a critical examination comparing microbial and macrobial agents. BioControl 58:575–593

    Article  CAS  Google Scholar 

  • Tambong JT, Höfte M (2001) Phenazines are involved in biocontrol of Pythium myriotylum on cocoyam by Pseudomonas aeruginosa PNA1. Eur J Plant Pathol 107:511–521

    Article  CAS  Google Scholar 

  • Tambong JT, Xu R (2013) Culture-independent analysis of Pseudomonas community structures in fertilized and unfertilized agricultural soils. Ann Microbiol 63:323–333

    Article  CAS  Google Scholar 

  • Thomashow LS, Weller DM, Bonsall RF, Pierson LS III (1990) Production of the antibiotic phenazine-1-carboxylic acid by fluorescent Pseudomonas species in the rhizosphere of wheat. Appl Environ Microbiol 56:908–912

    CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyay A, Srivastava S (2011) Phenazine-1-carboxylic acid is a more important contributor to biocontrol Fusarium oxysporum than pyrrolnitrin in Pseudomonas fluorescens strain Psd. Microbiol Res 166:323–335

    Article  CAS  PubMed  Google Scholar 

  • van Rij ET, Wesselink M, Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2004) Influence of environmental conditions on the production of phenazine-1-carboxamide by Pseudomonas chlororaphis PCL1391. Mol Plant Microbe Interact 17:557–566

    Article  PubMed  Google Scholar 

  • Varivarn K, Champa LA, Silby MW, Robleto EA (2013) Colonization strategies of Pseudomonas fluorescens Pf0-1: activation of soil-specific genes important for diverse and specific environments. BMC Microbiol 13:92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velivelli SLS, De Vos P, Kromann P, Declerck S, Prestwich BD (2014) Biological control agents: from field to market, problems, and challenges. Trends Biotechnol 32:493–496

    Article  CAS  PubMed  Google Scholar 

  • Vemmer M, Patel AV (2013) Review of encapsulation methods suitable for microbial biological control agents. Biol Control 67:380–389

    Article  CAS  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Viebahn M, Glandorf DCM, Ouwens TWM, Smit E, Leeflang P, Wernars K, Thomashow LS, van Loon LC, Bakker PAHM (2003) Repeated introduction of genetically modified Pseudomonas putida WCS358r without intensified effects on the indigenous microflora of field-grown wheat. Appl Environ Microbiol 69:3110–3118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15:22–30

    Article  CAS  PubMed  Google Scholar 

  • Voisard C, Keel C, Haas D, Défago G (1989) Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J 8:351–358

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Kern SE, Newman DK (2010) Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192:365–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wilks JC, Danhorn T, Ramos I, Croal L, Newman DK (2011) Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J Bacteriol 193:3606–3617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Yu JM, Pierson LS III, Pierson EA (2012) Differential regulation of phenazine biosynthesis by RpeA and RpeB in Pseudomonas chlororaphis 30–84. Microbiology 158:1745–1757

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Lee S-H, Seeve C, Yu JM, Pierson LS III, Pierson EA (2013) Roles of the Gac-Rsm pathway in the regulation of phenazine biosynthesis in Pseudomonas chlororaphis 30–84. Microbiol Open 2:505–524

    Article  CAS  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 

  • Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256

    Article  PubMed  Google Scholar 

  • Weller DM, Raaijmakers JM, McSpadden Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348

    Article  CAS  PubMed  Google Scholar 

  • Yang M-M, Mavrodi DV, Mavrodi OV, Bonsall RF, Parejko JA, Paulitz TC, Thomashow LS, Yang H-T, Weller DM, Guo J-H (2011) Biological control of take-all by fluorescent Pseudomonas spp. from Chinese wheat fields. Phytopathology 101:1481–1491. doi:10.1094/PHYTO-04-11-0096

    Article  PubMed  Google Scholar 

  • Zhang J, Wang W, Lu X, Xu Y, Zhang X (2010) The stability and degradation of a new biological pesticide, pyoluteorin. Pest Manag Sci 66:248–252

    Article  CAS  PubMed  Google Scholar 

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Arseneault, T., Filion, M. (2016). Phenazine-Producing Pseudomonas spp. as Biocontrol Agents of Plant Pathogens. In: Singh, D., Singh, H., Prabha, R. (eds) Microbial Inoculants in Sustainable Agricultural Productivity. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2644-4_4

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