Skip to main content

Advertisement

SpringerLink
Log in

Screening for candidate bacterial biocontrol agents against soilborne fungal plant pathogens

  • Review Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Over the years, many bacterial isolates have been evaluated as potential biocontrol agents against soilborne fungal phytopathogens. However, few of them were ultimately successful after evaluation in field trials. One of the major reasons for this failure is the lack of appropriate screening procedures to select the most suitable microorganisms for disease control in diverse soil environments. For this reason, the study of bacterial screening has a future that is characterised by many technical and conceptual challenges. In this review, we summarise and discuss the convenience of use of the main screening methods currently applied to select bacterial candidates for biocontrol of fungal and oomycete soilborne phytopathogens. Also, a comparative case study of the application of different screening methods applied to an experimental pathosystem is shown, revealing the success of bacterial candidates selected by different strategies for biocontrol of the phytopathogenic fungus Rosellinia necatrix in avocado plants. Screening for antagonism against this fungal pathogen, one of the more straightforward methods used for the selection of bacterial biocontrol agents, was proven to be a valid strategy for this experimental system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ajit NS, Verma R, Shanmugam V (2006) Extracellular chitinases of fluorescent pseudomonads antifungal to Fusarium oxysporum f. sp. dianthi causing carnation wilt. Curr Microbiol 52:310–316

    CAS  PubMed  Google Scholar 

  • Aravind R, Kumar A, Eapen SJ, Ramana (2009) Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: isolation, identification and evaluation against Phytophthora capsici. Lett Appl Microbiol 48:58–64

    CAS  PubMed  Google Scholar 

  • Aravind R, Eapen SJ, Kumar A, Dinu A, Ramana KV (2010) Screening of endophytic bacteria and evaluation of selected isolates for suppression of burrowing nematode (Radopholus similis Thorne) using three varieties of black pepper (Piper nigrum L.). Crop Protect 29:318–324

    Google Scholar 

  • Bakker PAHM, Ran LX, Pieterse CMJ, Van Loon LC (2003) Understanding the involvement of rhizobacteria-mediated induction of systemic resistance in biocontrol of plant diseases. Can J Plant Pathol 25:5–9

    Google Scholar 

  • Benitez MS, McSpadden Gardener BB (2009) Linking sequence to function in soil bacteria sequence-directed isolation of novel bacteria contributing to soilborne plant disease suppression. Appl Environ Microbiol 75:915–924

    CAS  PubMed  Google Scholar 

  • Berg G (2007) Biologcial control of fungal soilborne pathogens in strawberries. In: Chincholkar SB, Mukerji KG (eds) Biological control of plant diseases. The Haworth Press, Inc, Birghamton

    Google Scholar 

  • Berg G, Marten P, Minkwitz A, Brückner S (2001) Efficient biological control of fungal plant diseases by Streptomyces sp. DSMZ 12424. J Plant Dis Protect 108:1–10

    CAS  Google Scholar 

  • Bergsma-Vlami M, Prins ME, Raaijmakers JM (2005) Influence of plant species on population dynamics, genotypic diversity and antibiotic production in the rhizosphere by indigenous Pseudomonas spp. FEMS Microbiol Ecol 52:59–69

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Budi SW, van Tuinen D, Arnould C, Dumas-Gaudut E, Gianinazzi-Pearson V, Gianinazzi S (2000) Hydrolytic enzyme activity of Paenibacillus sp. strain B2 and effect of antagonistic bacterium on cell wall integrity of two soil-borne pathogenic fungi. Appl Soil Ecol 15:191–199

    Google Scholar 

  • Burkhead KD, Schisler DA, Slininger PJ (1995) Bioautography shows antibiotic production by soil bacterial isolates antagonistic to fungal dry rot of potatoes. Soil Biol Biochem 27:1611–1616

    CAS  Google Scholar 

  • Campbell R (1986) The search for biological control agents against plant pathogens: a pragmatic approach. Biol Agric Hortic 3:317–327

    Google Scholar 

  • Campbell R (1994) Biological control of soil-borne diseases: some present problems and different approaches. Crop Prot 13:4–13

    Google Scholar 

  • Cattelan ME, Hartel PG, Fuhrmann JJ (1999) Screening of plant growth-promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Amer 63:1670–1680

    CAS  Google Scholar 

  • Cazorla FM, Bloemberg GV, Lugtenberg BJJ (2001) Biocontrol of white root rot on avocado plants using rhizobacterial strains. IOBC/WPRS Bull 24:79–82

    Google Scholar 

  • Cazorla FM, Duckett SB, Berstrom ET, Noreen S, Odijk R, Lugtenberg BJJ, Thomas-Oates JE, Bloemberg GV (2006) Biocontrol of avocado Demathophora root rot by antagonistic Pseudomonas fluorescens PCL1606 correlates with the production of 2-hexyl 5-propyl resorcinol. Mol Plant-Microb Interact 19:418–428

    CAS  Google Scholar 

  • Cazorla FM, Romero D, Pérez-García A, Lugtenberg BJJ, de Vicente A, Bloemberg GV (2007) Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J Appl Microbiol 103:1950–1959

    CAS  PubMed  Google Scholar 

  • Chaiharn M, Chunhaleuchanon S, Lumyong S (2009) Screening siderophore producing bacteria as potential biological control agent for fungal rice pathogens in Thailand. World J Microbiol Biotech 25:1919–1928

    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-V, 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-Microb Interact 11:1069–1077

    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-Microb Interact 14:969–979

    CAS  Google Scholar 

  • Compant S, duffy B, Nowak J, Clément C, Ait Barka E (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    CAS  PubMed  Google Scholar 

  • Daayf F, Adam L, Fernando WGD (2003) Comparative screening of bacteria for biocontrol of potato late blight (strain US-8), using in-vitro, detached-leaves, and whole-plant testing systems. Can J Plant Pathol 25:276–284

    Google Scholar 

  • Deacon JW (1991) Significance of ecology in the development of biocontrol agents against soil-borne plant pathogens. Biocontrol Sci Technol 1:5–20

    Google Scholar 

  • Deacon JW (1994) Rhizosphere constraints affecting biocontrol organisms applied to seeds. In: Martin T (ed) BCPC monograph no 57: seed treatment: progress and prospects. BCPC Surrey, UK, pp 315–326

    Google Scholar 

  • de Boer W, Leveau JH, Kowalchuk GA, Gunnewiek PJAK, Abeln ECA, Figge MJ, Sjollema K, Janse JD, van Veen JA (2004) Collimonas fungivorans gen. nov., sp. nov., a chitinolytic soil bacterium with the ability to grow on living fungal hyphae. J Syst Evol Microbiol 54:857–864

    Google Scholar 

  • de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacteria niche developments. FEMS Microbiol Rev 29:795–811

    PubMed  Google Scholar 

  • de Weert S, Bloemberg GV (2006) Rhizosphere competence and the role of root colonization in biocontrol. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 317–333

    Google Scholar 

  • de Weert S, Kuiper I, Langedijk EL, Lamers GEM, Lugtenberg BJJ (2004) Role of chemotaxis toward fusaric acid in colonization of hyphae of Fusarium oxysporum f.sp. radicis-lycopersici by Pseudomonas fluorescens WCS365. Mol Plant-Microb Interact 17:1185–1191

    Google Scholar 

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

    PubMed  Google Scholar 

  • Duczek LJ (1994) Relationship between a greenhouse and field assay for biological control of common root rot of spring wheat and barley. Can Plant Dis Surv 74:135–140

    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

    CAS  PubMed  Google Scholar 

  • Duffy B, Schouten A, Raaijmakers JM (2003) Pathogen self-defence: mechanisms to counteract microbial antagonism. Annu Rev Phytopathol 41:501–538

    CAS  PubMed  Google Scholar 

  • Dunne C, Moenne-Loccoz Y, de Bruijin FJ, O’Gara F (2000) Overproduction of an inducible extracellular serine protease improves biological control of Pythium ultimum by Stenotromonas maltophilia strain W81. Microbiol 146:2069–2078

    CAS  Google Scholar 

  • Egamberdieva D, Kucharova Z (2009) Selection for root colonizing bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45:563–571

    Google Scholar 

  • Elad Y, Chet I (1995) Practical approaches for biocontrol implementation. In: Reuveni R (ed) Novel approaches to integrated pest management. Lewis Publishers, CRC Press, Boca Raton, pp 323–338

    Google Scholar 

  • Faltin F, Lottmann J, Grosch R, Berg G (2004) Strategy to select and assess antagonistic bacteria for biological control of Rhizoctonia solani Kühn. Can J Microbiol 50:811–820

    CAS  PubMed  Google Scholar 

  • Folman LB, Postma J, Van Veen JA (2003) Inability to find consistent bacterial biocontrol agents of Pythium aphanidermatum in cucumber using screens based on ecophysiological traits. Microbial Ecol 45:72–87

    CAS  Google Scholar 

  • Frankowski J, Lorito M, Scala F, Schmidt R, Berg G, Bahl H (2001) Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Arch Microbiol 176:421–426

    CAS  PubMed  Google Scholar 

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

    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 rhizospere. World J Microbiol Biotech 17:51–55

    CAS  Google Scholar 

  • González-Sánchez MA, Pérez-Jiménez RM, Pliego C, Ramos C, de Vicente A, Cazorla FM (2010) Biocontrol bacteria selected by a direct plant protection strategy againt avocado white root rot show antagonism as a prevalent trait. J Appl Microbiol 109:65–78

    PubMed  Google Scholar 

  • Guetsky R, Shtienberg D, Elad Y, Fischer E, Dinoor A (2002) Improving biological control by combining biocontrol agents each with several mechanisms of disease suppression. Phytopathology 92:976–988

    PubMed  Google Scholar 

  • Gross H, Loper JE (2009) Genomic of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 26:1408–1446

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hogan DA, Kolter R (2002) Pseudomonas–Candida interactions: an ecological role for virulence factors. Science 296:2229–2232

    CAS  PubMed  Google Scholar 

  • Hoster F, Schmitz JE, Daniel R (2005) Enrichment of chitinolytic microorganisms: isolation and characterization of a chitinase exhibiting antifungal activity against phytopathogenic fungi from a novel Streptomyces strain. Appl Microbiol Biotechnol 66:434–442

    CAS  PubMed  Google Scholar 

  • Howell CR, Stipanovic RD (1980) Suppression of Pythium ultimum induced damping off cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Phytopathology 70:712–715

    CAS  Google Scholar 

  • Howell CR, Beier RC, Stipanovic RD (1988) Production of ammonia by Enterobacter cloacae and its possible role in the biological control of Pythium preemergence damping-off by the bacterium. Phytopathology 78:1075–1078

    CAS  Google Scholar 

  • Kageyama K, Nelson EB (2003) Differential inactivation of seed exudates stimulation of Pythium ultimum sporangium germination by Enterobacter cloacae influences biological control efficacy on different plant species. Appl Environ Microbiol 69:1114–1120

    CAS  PubMed  Google Scholar 

  • Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg BJJ (2005) Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7:1809–1817

    CAS  PubMed  Google Scholar 

  • Kamilova F, Leveau JHJ, Lugtenberg BJJ (2007) Collimonas fungivorans, an unpredicted in vitro but efficient in vivo biocontrol agent for the suppression of tomato foot and root rot. Environ Microbiol 9:1597–1603

    CAS  PubMed  Google Scholar 

  • Kanadani G, Date H, Nasu H (1998) Effect of fluazinam soil-drench on white root rot of grapevine. Ann Phytopathol Soc Jpn 64:139–141

    CAS  Google Scholar 

  • Kilic-Ekici O, Yuen GY (2003) Induced resistance as a mechanisms of biological control by Lysobacter enzymogenes strain C3. Phytopathology 93:1103–1110

    PubMed  Google Scholar 

  • Kinsella K, Schulthess CP, Morris TF, Stuart JD (2009) Rapid quantification of Bacillus subtilis antibiotics in the rhizosphere. Soil Biol Biochem 41:374–379

    CAS  Google Scholar 

  • Kloepper JW (1991) Development of in vivo assays for prescreening antagonists of Rhizoctonia solani on cotton. Phytopathology 81:1006–1013

    Google Scholar 

  • Kloepper JW, Schroth MN (1981) Relationship of in vitro antibiosis of plant growth-promoting rhizobacteria to enhanced plant growth and the displacement of root microflora. Phytopathology 71:1020–1024

    Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus. Phytopathology 94:1259–1266

    CAS  PubMed  Google Scholar 

  • Knudsen IMB, Hockenhull J, Jensen DF, Gerhardson B, Hökeberg M, Tahvonen R, Teperi E, Sundheim L, Henriksen B (1997) Selection of biological control agents for controlling soil and seed-borne diseases in the field. Eur J Plant Pathol 103:775–784

    Google Scholar 

  • Kobayashi DY, Reedy RM, Bick JA, Oudemans PV (2002) Characterization of a chitinase gene from Stenotrophomonas maltophilia strain 34 S1 and its involvement in biological control. Appl Environ Microbiol 68:1047–1054

    CAS  PubMed  Google Scholar 

  • Köhl J (2009) Screening of biocontrol agents for control of foliar diseases. In: Recent Developments in Management of Plant Diseases, U. Gisi et al (Eds) Plant Pathology in the 21st Century 1, doi:10.1007/978-1-4020-8804-9_9, Springer Science + Business Media B.V

  • Kommedahl T, Windels CE (1978) Evaluation of biological seed treatment for controlling root diseases of pea. Phytopathology 68:1087–1095

    Google Scholar 

  • Koumoutsi A, Chen XH, Henne A, Liesegang H, Gabriele H, Franke P, Vater J, Borris R (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186:1084–1096

    CAS  PubMed  Google Scholar 

  • Landa BB, Mavrodi OV, Raaijmakers JM, McSpadden-Gardener BB, Thomashow LS, Weller DM (2002) Differential ability of genotypes of 2, 4-diacetylphloroglucinol- producing Pseudomonas fluorescens strains to colonize the roots of pea plants. Appl Environ Microbiol 68:3226–3237

    CAS  PubMed  Google Scholar 

  • Larkin RP, Fravel DR (1998) Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Plant Dis 82:1022–1028

    Google Scholar 

  • Leveau JHJ, Preston GM (2008) Bacterial mycophagy: definition and diagnosis of a unique bacterial-fungal interaction. New Phytologist 177:859–876

    PubMed  Google Scholar 

  • Leveau JHJ, Gerards S, Fritsche K, Zondag G, van Veen JA (2006) Genomic flank-sequencing of plasposon insertion sites for rapid identification of functional genes. J Microbiol Methods 66:276–285

    CAS  PubMed  Google Scholar 

  • Li S, Jochum CC, Yu F, Zaleta-Rivera K, Du L, Harris SD, Yuen GY (2008) An antibiotic complex from Lysobacter enzymogenes strain C3: antimicrobial activity and role in plant disease control. Phytopathology 98:695–701

    CAS  PubMed  Google Scholar 

  • Loper JE, Gross H (2007) Genomic analysis of antifungal metabolite production by Pseudomonas fluorescens Pf-5. Eur J Plant Pathol 119:265–278

    CAS  Google Scholar 

  • Loper JE, Henkels MD (1999) Utilization of heterologous siderophores enhanced levels of iron available to Pseudomonas putida in the rhizosphere. Appl Environ Microbiol 65:5357–5363

    CAS  PubMed  Google Scholar 

  • Loper JE, Kobayashi DY, Paulsen IT (2007) The genomic sequence of Pseudomonas fluorescens Pf-5: insight into biological control. Phytopathology 97:233–238

    CAS  PubMed  Google Scholar 

  • López-Herrera CJ, Pérez-Jiménez RM, Zea-Bonilla T, Basallote-Ureba MJ, Melero-Vara JM (1998) Soil solarization in established avocado trees for control of Dematophora necatrix. Plant Dis 82:1088–1092

    Google Scholar 

  • Lugtenberg BJJ, Bloemberg GV (2004) Life in the rhizosphere. In: Ramos JL (ed) Pseudomonas. Kluwer Acad./Plenum, New York, 1:403–430

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lumsden RD, Lewis JA (1989) Selection, production, formulation and commercial use of plant disease biocontrol fungi: problems and progress. In: Whipps JM, Lumsden RD (eds) Biotechnology of fungi for improving plant growth. Cambridge University Press, Cambridge, pp 171–190

    Google Scholar 

  • Lumsden RD, Locke JC, Walter JF (1992) Isolation and localization of the antibiotic gliotoxin produced by Gliocladium virens from alginate prill in soil and soilless media. Phytopathology 82:230–235

    CAS  Google Scholar 

  • Martínez-Granero F, Rivilla R, Martín M (2006) Rhizosphere selection of highly motile phenotypic variants of Pseudomonas fluorescens with enhanced competitive colonization ability. Appl Environ Microbiol 72:3429–3434

    PubMed  Google Scholar 

  • McSppaden-Gardener BB, Fravel DR (2002) Biological control of plant pathogens: research, commercialization, and application in the USA. Plant Health Progress. doi:10.1094/PHP-2002-0510-01-RV

    Google Scholar 

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

    PubMed  Google Scholar 

  • Merriman P, Russell K (1990) Screening strategies for biological control. In: Hornby D (ed) Biological control of soil-borne plant pathogens. CAB International, Wallingford, pp 427–435

    Google Scholar 

  • Meyers SLF, Roberts DP (2002) Combinations of biocontrol agents for management of plant-parasitic nematodes and soilborne plant-pathogenic fungi. J Nematol 34:1–8

    Google Scholar 

  • Nürnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345

    PubMed  Google Scholar 

  • Ongena M, Duby F, Rossignol F, Fouconnier ML, Dommes J, Thonart P (2004) Stimulation of the lipoxygenase pathway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Mol Plant-Microb Interact 17:1009–1018

    CAS  Google Scholar 

  • Pal KK, McSpadden Gardener B (2006) Biological control of plant pathogens. The Plant Health Instructor. doi:10.1094/PHI-A-2006-1117-02. 25 pp

  • Pang Y, Liu X, Ma Y, Chernin L, Berg G, Gao K (2009) Induction of systemic resistance, root colonisation and biocontrol activities of the rhizospheric strain of Serratia plymuthica are dependen ton N-acyl homoserine lactones. Eur J Plant Pathol 124:261–268

    CAS  Google Scholar 

  • Péchy-Tarr M, Bruck DJ, Maurhofer M, Fichser E, Vogne C, Henkels MD, Donahue KM, Grunder J, Loper JE, Keel C (2008) Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ Microbiol 10:2368–2386

    PubMed  Google Scholar 

  • Pliego C, Cazorla FM, González-Sánchez MA, Pérez-Jiménez RM, de Vicente A, Ramos C (2007) Selection for biocontrol bacteria antagonistic toward Rosellinia necatrix by enrichment of competitive avocado root tip colonizers. Res Microbiol 158:463–470

    CAS  PubMed  Google Scholar 

  • Pliego C, de Weert S, Lamers G, de Vicente A, Bloemberg GV, Cazorla FM, Ramos C (2008) Two similar enhanced root-colonizing Pseudomonas strains differ largely in their colonization strategies of avocado roots and Rosellinia necatrix hyphae. Environ Microbiol 10:3295–3304

    PubMed  Google Scholar 

  • Pliego C, Kanematsu S, Ruano-Rosa D, de Vicente A, López-Herrera C, Cazorla FM, Ramos C (2009) GFP sheds light on the infection process of avocado roots by Rosellinia necatrix. Fungal Genet Biol 46:137–145

    CAS  PubMed  Google Scholar 

  • Prieto P, Navarro-Raya C, Valverde-Corredor A, Amyotte SG, Dobinson KF, Mercado-Blanco J (2009) Colonization process of olive tissues by Verticillium dahliae and its in planta interaction with the biocontrol root endophyte Pseudomonas fluorescens PICF7. Microb Biotechnol 2:499–511

    CAS  PubMed  Google Scholar 

  • Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek 81:537–547

    CAS  PubMed  Google Scholar 

  • Raaijmakers JM, de Bruijn I, de Kock MJD (2006) Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol Plant-Microb Interact 19:699–710

    CAS  Google Scholar 

  • Raupach GS, Kloepper JW (1998) Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88:1158–1164

    CAS  PubMed  Google Scholar 

  • Renwick A, Campbell R, Coe S (1991) Assessment of in vivo screening systems for potential biocontrol agents of Gaeumannomyces graminis. Plant Pathol 40:524–532

    Google Scholar 

  • Roberts DP, Lohrke SM, Meyers SLF, Buyer JS, Bowers JH, Baker CJ, Li W, de Souza JT, Lenis JA, Chung S (2005) Biocontrol agents applied individually and in combination for suppression of soilborne diseases of cucumber. Crop Prot 24:141–155

    Google Scholar 

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

    CAS  Google Scholar 

  • Romero D, de Vicente A, Rakotoaly RV, Dufour SE, Veening JW, Arrebola E, Cazorla FM, Kuipers OP, Paquot M, Pérez-García A (2007) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis towards Podosphaera fusca. Mol Plant-Microb Interact 20:430–440

    CAS  Google Scholar 

  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner H-Y, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    CAS  PubMed  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026

    CAS  PubMed  Google Scholar 

  • Schroth MN, Hancock JG (1982) Disease-suppressive soil and root-colonizing bacteria. Science 216:1376–1381

    CAS  PubMed  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Ann Biochem 160:47–56

    CAS  Google Scholar 

  • Sessitsch A, Reiter B, Berg G (2004) Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can J Microbiol 50:239–249

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol. doi:10.1146/annurev-phyto-073009-114450

    PubMed  Google Scholar 

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

    Google Scholar 

  • Someya N, Tsuchiya K, Yoshida T, Noguchi MT, Akutsu K, Sawada H (2007) Fungal cell wall degrading enzyme-producing bacterium enhances the biocontrol efficacy of antibiotic-producing bacterium against cabbage yellows. J Plant Dis Protect 114:108–112

    Google Scholar 

  • Sztejnberg A, Madar Z (1980) Host range of Dematophora necatrix, the cause of white root rot disease in fruit trees. Plant Dis 64:662–664

    Google Scholar 

  • Sztejnberg A, Omary N, Pinkas Y (1983) Control of Rosellinia necatrix by deep placement and hot treatment with methyl bromide. EPPO Bull 13:483–485

    Google Scholar 

  • Sztejnberg A, Freeman S, Chet I, Katan J (1987) Control of Rosellinia necatrix in soil and in orchards by solarization and Trichoderma harzianum. Plant Dis 71:365–369

    Google Scholar 

  • Ten Hoopen GM, Krauss U (2006) Biology and control of Rosellinia bunodes, Rosellinia necatrix and Rosellinia pepo: a review. Crop Prot 25:89–107

    Google Scholar 

  • Thomashow LS, Weller DM (1996) Current concepts in the use of introduced bacteria for biological disease control: mechanisms and antifungal metabolites. In: Stacy G, Keen N (eds) Plant-microbe interactions, vol. 1., pp 187–235

  • Tjamos EC, Tsitsigiannis DI, Tjamos SE, Antoniou PP, Katinakis P (2004) Selection and screening of endorhizosphere bacteria from solarized soils as biocontrol agents against Verticillium dahliae of solanaceous host. Eur J Plant Pathol 110:35–44

    CAS  Google Scholar 

  • Trejo-Estrada SR, Paszczynski A, Crawford DL (1998) Antibiosis and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9. Industrial Microbiol Biotech 21:81–90

    CAS  Google Scholar 

  • Validov S, Kamilova F, Lugtenberg BJJ (2009) Pseudomonas putida strain PCL1760 controls tomato foot and root rot in stonewool under industrial conditions in a certified greenhouse. Biol Control 48:6–11

    Google Scholar 

  • van Dijk K, Nelson EB (2000) Fatty acid competition as a mechanism by which Enterobacter cloacae suppresses Pythium ultimum sporangium germination and damping-off. Appl Environ Microbiol 66:5340–5347

    PubMed  Google Scholar 

  • van Loon LC (2007) Plant responses to plant growth-promoting bacteria. Eur J Plant Pathol 119:243–254

    Google Scholar 

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

    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-Microb Interact 17:557–566

    Google Scholar 

  • van Rij ET, Girard G, Lugtenberg BJJ, Bloemberg GV (2005) Influence of fusaric acid on phenazine-1-carboxamide synthesis and gene expression of Pseudomonas chlororaphis PCL1391. Microbiology 151:2805–2814

    PubMed  Google Scholar 

  • Vicedo B, Peñalver R, Asins MJ, Lopez MM (1993) Biological control of Agrobacterium tumefaciens, colonization, and pAgK84 transfer with Agrobacterium radiobacter K84 and the Tra- mutant strain K1026. Appl Environ Microbiol 59:309–315

    CAS  PubMed  Google Scholar 

  • Viterbo A, Ramot O, Chernin L, Chet I (2002) Significance of lytic enzymes from Trichoderma spp in the biocontrol of fungal plant pathogens. Antonie Van Leeuwenhoek 81:549–556

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Whipps JM (1997) Ecological considerations involved in commercial development of biological control agents for soil-borne diseases. In: van Elsas JD, Wellington EMH, Trevors JT (eds) Modern soil microbiology. Elsevier, The Netherlands

    Google Scholar 

  • Winding A, Binnerup SJ, Pritchard H (2004) Non-target effects of bacterial biological control agents suppressing root pathogenic fungi. FEMS Microbiol Ecol 47:129–141

    CAS  PubMed  Google Scholar 

  • Wu Y, Lu C, Qian X, Huang Y, Shen Y (2009) Diversities within genotypes, bioactivity and biosynthetic genes of endophytic actinomycetes isolated from three pharmaceutical plants. Curr Microbiol 59:475–482

    CAS  PubMed  Google Scholar 

  • Zachow C, Priker H, Westendorf C, Tilcher R, Berg G (2009) The Caenorhabditis elegans assay: a tool to evaluate the pathogenic potential of bacterial biocontrol agents. Eur J Plant Pathol 125:367–376

    CAS  Google Scholar 

  • Zhang Z, Yuen GY (2000) The role of chitinase production by Stenotrophomonas maltophilia strain C3 in biological control of Bipolaris sorokiniana. Phytopathology 90:384–389

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research has been supported by the Spanish Plan Nacional I+D+I Grants AGL 2005-06347-C03-01 and AGL 2008-05453-C02-01, and by the Junta de Andalucía Grant AGR-169, and cofinanced by EU (FEDER).

Author information

Authors and Affiliations

  1. Área de Genética, Instituto de Hortofruticultura Subtropical y Mediterránea, Universidad de Málaga (IHSM-UMA-CSIC), Facultad de Ciencias, Campus Universitario de Teatinos, s/n, E-29071, Málaga, Spain

    Clara Pliego & Cayo Ramos

  2. Departamento de Microbiología, Instituto de Hortofruticultura Subtropical y Mediterránea, Universidad de Málaga (IHSM-UMA-CSIC), Facultad de Ciencias, Campus Universitario de Teatinos, s/n, E-29071, Málaga, Spain

    Antonio de Vicente & Francisco M. Cazorla

Authors
  1. Clara Pliego
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cayo Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antonio de Vicente
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francisco M. Cazorla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francisco M. Cazorla.

Additional information

Responsible Editor: Peter A. H. Bakker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pliego, C., Ramos, C., de Vicente, A. et al. Screening for candidate bacterial biocontrol agents against soilborne fungal plant pathogens. Plant Soil 340, 505–520 (2011). https://doi.org/10.1007/s11104-010-0615-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-010-0615-8

Keywords

Search

Navigation