Advertisement

Pseudomonas and other Microbes in Disease-Suppressive Soils

  • Martina Kyselková
  • Yvan Moënne-LoccozEmail author
Chapter
Part of the Sustainable Agriculture Reviews book series (SARV, volume 9)

Abstract

Soil-borne phytopathogens cause extensive damage to cultivated plants worldwide, resulting in yield loss worth billions of Euros each year. Soil fumigation is the most effective chemical treatment but is too expensive for many crops, and fumigants like methyl bromide are being phased out for environmental reasons. In this context, much is to be learned from disease-suppressive soils, where susceptible plants are protected from soil-borne pathogens by the indigenous microbiota, because these microbial interactions may be exploited to design sustainable crop protection strategies for ordinary farm soils. However, our knowledge of plant-protecting microorganisms and biocontrol mechanisms involved in soil suppressiveness remain very fragmented, as most knowledge on disease suppressive soils comes from studies restricted to individual plant-protecting microbial populations, mostly fluorescent Pseudomonas species. The phenomenon of disease suppressiveness remains therefore poorly understood, even in the most studied cases such as suppressiveness to wheat take-all.

We reviewed the respective biocontrol contributions of fluorescent pseudomonads and other plant-protecting microorganisms in disease-suppressive soils. The ability to inhibit soil-borne pathogens and to protect plants occurs both in Pseudomonas and non-Pseudomonas microorganisms, including diverse bacteria and fungi, and both play important roles in soil suppressiveness. In Pseudomonas, antibiosis and competition were shown to be important mechanisms of pathogen suppression, though direct effects on plant, e.g. induced systemic resistance, phytohormone interference and plant-growth promotion, were also reported. These types of mechanisms occur also in non-Pseudomonas biocontrol microbes, some of them also displaying hyperparasitism in certain types of suppressive soils.

This review shows that in suppressive soils where Pseudomonas play an important role, the roles of non-Pseudomonas microorganisms were often neglected, and vice versa. Yet, Pseudomonas and other microorganisms may interact with each other in the rhizosphere and with the plant, and some recent studies indicate that disease suppressiveness is an emerging soil property that can typically result from these multiple interactions. In conclusion, we propose that a parallel assessment of Pseudomonas and non-Pseudomonas microorganisms in suppressive soils, e.g. using microarrays or metagenomics, may bring a better understanding of disease suppressiveness.

Keywords

Biocontrol Disease-suppressive soil Plant pathogen Pseudomonas Rhizosphere 

Notes

Acknowledgement

This work was supported by CORESTA (Paris, France), the bi-national PHC program Barrande (Agentura Inovačního Podnikání, Prague, Czech Republic, and EGIDE), the Ministry of Agriculture of the Czech Republic (project NAZV QH 92151), the Ministère Français de la Recherche, the Bureau des Ressources Génétiques (BRG; Paris, France), and the European Union (FW6 STREP project MicroMaize). We thank K. Schreiner, M. Schloter (German Research Center for Environmental Health, Helmholtz Zentrum München, Germany), M. Frapolli and G. Défago (Institute of Integrative Biology, Swiss Federal Institute of Technology, Zurich, Switzerland) for sharing unpublished information, and C. Prigent-Combaret (UMR CNRS 5557 Ecologie microbienne, Université Lyon 1, Villeurbanne, France) for providing Fig. 3.

References

  1. Abadie C, Edel V, Alabouvette C (1998) Soil suppressiveness to Fusarium wilt: influence of a cover-plant on density and diversity of Fusarium populations. Soil Biol Biochem 30:643–649CrossRefGoogle Scholar
  2. Agrios GN (1997) Plant pathology. Academic, San DiegoGoogle Scholar
  3. Alabouvette C (1986) Fusarium-wilt suppressive soils from the Châteaurenard region – review of a 10-year study. Agronomie 6:273–284CrossRefGoogle Scholar
  4. Altomare C, Norvell WA, Bjorkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Appl Environ Microbiol 65:2926–2933PubMedGoogle Scholar
  5. Anderson LM, Stockwell VO, Loper JE (2004) An extracellular protease of Pseudomonas fluorescens inactivates antibiotics of Pantoea agglomerans. Phytopathology 94:1228–1234PubMedCrossRefGoogle Scholar
  6. Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: Effect on radishes (Raphanus sativus L.). Plant Soil 204:57–67CrossRefGoogle Scholar
  7. Asaka O, Shoda M (1996) Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl Environ Microbiol 62:4081–4085PubMedGoogle Scholar
  8. Azcón-Aguilar C, Barea MJ (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved. Mycorrhiza 6:457–464CrossRefGoogle Scholar
  9. Baayen RP, O’Donnell K, Bonants PJM, Cigelnik E, Kroon LPNM, Roebroeck EJA, Waalwijk C (2000) Gene genealogies and AFLP analyses in the Fusarium oxysporum complex identify monophyletic and nonmonophyletic formae speciales causing wilt and rot disease. Phytopathology 90:891–900PubMedCrossRefGoogle Scholar
  10. Baker KF, Cook RJ (1974) Biological control of plant pathogens. Freeman, San FranciscoGoogle Scholar
  11. Bally R, Elmerich C (2007) Biocontrol of plant diseases by associative and endophytic nitrogen-fixing bacteria. In: Elmerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer, Dordrecht, pp 171–190Google Scholar
  12. Banik S, Dey B (1982) Available phosphate content of an alluvial soil as influenced by inoculation of some isolated phosphate-solubilizing micro-organisms. Plant Soil 69:353–364CrossRefGoogle Scholar
  13. Bansal RK, Dahiya RS, Narula N, Jain RK (2005) Management of Meloidogyne incognita in cotton, using strains of the bacterium Gluconacetobacter diazotrophicus. Nematol Medit 33:101–105Google Scholar
  14. Barea JM, Andrade G, Bianciotto V, Dowling D, Lohrke S, Bonfante P, O’Gara F, Azcon-Aguilar C (1998) Impact on arbuscular mycorrhiza formation of Pseudomonas strains used as inoculants for biocontrol of soil-borne fungal plant pathogens. Appl Environ Microbiol 64:2304–2307PubMedGoogle Scholar
  15. Barret M, Frey-Klett P, Boutin M, Guillerm-Erckelboudt A-Y, Martin F, Guillot L, Sarniguet A (2009) The plant pathogenic fungus Gaeumannomyces graminis var. tritici improves bacterial growth and triggers early gene regulations in the biocontrol strain Pseudomonas fluorescens Pf29Arp. New Phytol 181:435–447PubMedCrossRefGoogle Scholar
  16. Bastián F, Cohen A, Piccoli P, Luna V, Bottini R, Baraldi R, Bottini R (1998) Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media. Plant Growth Regul 24:7–11CrossRefGoogle Scholar
  17. Becker DM, Kinkel LL, Schottel JL (1997) Evidence for interspecies communication and its potential role in pathogen suppression in a naturally occurring disease suppressive soil. Can J Microbiol 43:985–990CrossRefGoogle Scholar
  18. Benhamou N, Gagné S, Le Quéré D, Dehbi L (2000) Bacterial-mediated induced resistance in cucumber: beneficial effect of the endophytic bacterium Serratia plymuthica on the protection against infection by Pythium ultimum. Phytopathology 90:45–56PubMedCrossRefGoogle Scholar
  19. Benítez M-S, 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 75:915–924PubMedCrossRefGoogle Scholar
  20. Berg G (2000) Diversity of antifungal and plant-associated Serratia plymuthica strains. J Appl Microbiol 88:952–960PubMedCrossRefGoogle Scholar
  21. Bergen WG, Bates DB (1984) Ionophores: their effect on production efficiency and mode of action. J Anim Sci 58:1465–1483PubMedGoogle Scholar
  22. Berry LA, Jones EE, Deacon JW (1993) Interaction of the mycoparasite Pythium oligandrum with other Pythium species. Biocontrol Sci Technol 3:247–260CrossRefGoogle Scholar
  23. Bevivino A, Sarrocco S, Dalmastri C, Tabacchioni S, Cantale C, Chiarini L (1998) Characterization of a free-living maize-rhizosphere population of Burkholderia cepacia: effect of seed treatment on disease suppression and growth promotion of maize. FEMS Microbiol Ecol 27:225–237CrossRefGoogle Scholar
  24. Beyeler M, Keel C, Michaux P, Haas D (1999) Enhanced production of indole-3-acetic acid by a genetically modified strain of Pseudomonas fluorescens CHA0 affects root growth of cucumber, but does not improve protection of the plant against Pythium root rot. FEMS Microbiol Ecol 28:225–233CrossRefGoogle Scholar
  25. Blaha D, Prigent-Combaret C, Sajjad MM, Moënne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470PubMedCrossRefGoogle Scholar
  26. Bolwerk A, Lagopodi AL, Lugtenberg BJJ, Bloemberg GV (2005) Visualization of interactions between a pathogenic and a beneficial Fusarium strain during biocontrol of tomato foot and root rot. Mol Plant-Microbe Interact 18:710–721PubMedCrossRefGoogle Scholar
  27. Bordoloi GN, Kumari B, Guha A, Thakur D, Bordoloi M, Roy MK, Bora TC (2002) Potential of a novel antibiotic, 2-methylheptyl isonicotinate, as a biocontrol agent against fusarial wilt of crucifers. Pest Manag Sci 58:297–302PubMedCrossRefGoogle Scholar
  28. Borneman J, Becker JO (2007) Identifying microorganisms involved in specific pathogen suppression in soil. Annu Rev Phytopathol 45:153–172PubMedCrossRefGoogle Scholar
  29. Bowers JH, Kinkel LL, Jones RK (1996) Influence of disease-suppressive strains of Streptomyces on the native Streptomyces community in soil as determined by the analysis of cellular fatty acids. Can J Microbiol 42:27–37PubMedCrossRefGoogle Scholar
  30. Brazelton JN, Pfeufer EE, Sweat TA, McSpadden Gardener BB, Coenen C (2008) 2,4-diacetylphloroglucinol alters plant root development. Mol Plant-Microbe Interact 21:1349–1358PubMedCrossRefGoogle Scholar
  31. Budi SW, van Tuinen D, Arnould C, Dumas-Gaudot E, Gianinazzi-Pearson V, Gianinazzi S (2000) Hydrolytic enzyme activity of Paenibacillus sp. strain B2 and effects of the antagonistic bacterium on cell integrity of two soil-borne pathogenic fungi. Appl Soil Ecol 15:191–199CrossRefGoogle Scholar
  32. Burr TJ, Reid CL (1994) Biological control of grape crown gall with non-tumorigenic Agrobacterium vitis strain F2/5. Am J Enol Vitic 45:213–219Google Scholar
  33. Carroll H, Moënne-Loccoz Y, Dowling DN, O’Gara F (1995) Mutational disruption of the biosynthesis genes coding for the antifungal metabolite 2,4-diacetylphloroglucinol does not influence the ecological fitness of Pseudomonas fluorescens F113 in the rhizosphere of sugar-beets. Appl Environ Microbiol 61:3002–3007PubMedGoogle Scholar
  34. Cartwright DK, Chilton WS, Benson DM (1995) Pyrrolnitrin and phenazine production by Pseudomonas cepacia, strain 5.5b, a biocontrol agent of Rhizoctonia solani. Appl Microbiol Biotechnol 43:211–216CrossRefGoogle Scholar
  35. Cavaglieri L, Orlando J, Rodríguez MI, Chulze S, Etcheverry M (2005) Biocontrol of Bacillus subtilis against Fusarium verticillioides in vitro and at the maize root level. Res Microbiol 156:748–754PubMedCrossRefGoogle Scholar
  36. Cavaglieri LR, Passone A, Etcheverry MG (2004) Correlation between screening procedures to select root endophytes for biological control of Fusarium verticillioides in Zea mays L. Biol Control 31:259–267CrossRefGoogle Scholar
  37. Cazar ME, Schmeda-Hirschmann G, Astudillo L (2005) Antimicrobial butyrolactone I derivatives from the Ecuadorian soil fungus Aspergillus terreus Thorn. var terreus. World J Microbiol Biotechnol 21:1067–1075CrossRefGoogle Scholar
  38. Chapon A, Guillerm AY, Delalande L, Lebreton L, Sarniguet A (2002) Dominant colonisation of wheat roots by Pseudomonas fluorescens Pf29A and selection of the indigenous microflora in the presence of the take-all fungus. Eur J Plant Pathol 108:449–459CrossRefGoogle Scholar
  39. Chen F, Guo YB, Wang JH, Li JY, Wang HM (2007) Biological control of grape crown gall by Rahnella aquatilis HX2. Plant Dis 91:957–963CrossRefGoogle Scholar
  40. Chen ZX, Dickson DW, McSorley R, Mitchell DJ, Hewlett TE (1996) Suppression of Meloidogyne arenaria race 1 by soil application of endospores of Pasteuria penetrans. J Nematol 28:159–168PubMedGoogle Scholar
  41. Chernin L, Ismailov Z, Haran S, Chet I (1995) Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl Environ Microbiol 61:1720–1726PubMedGoogle Scholar
  42. Chernin L, Brandis A, Ismailov Z, Chet I (1996) Pyrrolnitrin production by an Enterobacter agglomerans strain with a broad spectrum of antagonistic activity towards fungal and bacterial phytopathogens. Curr Microbiol 32:208–212CrossRefGoogle Scholar
  43. Chet I, Harman GE, Baker R (1981) Trichoderma hamatum: its hyphal interactions with Rhizoctonia solani and Pythium spp. Microb Ecol 7:29–38CrossRefGoogle Scholar
  44. Chin-A-Woeng TFC, Bloemberg GV, Mulders IHM, Dekkers LC, Lugtenberg BJJ (2000) Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol Plant-Microbe Interact 13:1340–1345PubMedCrossRefGoogle Scholar
  45. Cho J-C, Tiedje JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66:5448–5456PubMedCrossRefGoogle Scholar
  46. Cook JR, Baker KF (1983) The nature and practice of biological control of plant pathogens. American Phytopathological Society, St. PaulGoogle Scholar
  47. Cook RJ, Thomashow LS, Weller DM, Fujimoto D, Mazzola M, Bangera G, Kim D (1995) Molecular mechanisms of defense by rhizobacteria against root disease. Proc Natl Acad Sci USA 92:4197–4201PubMedCrossRefGoogle Scholar
  48. Coombs JT, Michelsen PP, Franco CMM (2004) Evaluation of endophytic actinobacteria as antagonists of Gaeumannomyces graminis var. tritici in wheat. Biol Control 29:359–366CrossRefGoogle Scholar
  49. Cosette P, Rebuffat S, Bodo B, Molle G (1999) The ion-channel activity of longibrachins LGA I and LGB II: effects of Pro-2/Ala and Gln-18/Glu substitutions on the alamethicin voltage-gated membrane channels. Biochim Biophys Acta – Biomembr 1461:113–122CrossRefGoogle Scholar
  50. 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 48:505–512PubMedCrossRefGoogle Scholar
  51. Crawford DL, Lynch JM, Whipps JM, Ousley MA (1993) Isolation and characterization of actinomycete antagonists of a fungal root pathogen. Appl Environ Microbiol 59:3899–3905PubMedGoogle Scholar
  52. Cronin D, Moënne-Loccoz Y, Dunne C, O’Gara F (1997a) Inhibition of egg hatch of the potato cyst nematode Globodera rostochiensis by chitinase-producing bacteria. Eur J Plant Pathol 103:433–440CrossRefGoogle Scholar
  53. Cronin D, Moënne-Loccoz Y, Fenton A, Dowling DN, O’Gara F (1997b) Ecological interaction of a biocontrol Pseudomonas fluorescens strain producing 2,4-diacetylphloroglucinol with the soft rot potato pathogen Erwinia carotovora subsp. atroseptica. FEMS Microbiol Ecol 23:95–106CrossRefGoogle Scholar
  54. Cronin D, Moënne-Loccoz Y, Fenton A, Dunne C, Dowling DN, O’Gara F (1997c) Role of 2,4-diacetylphloroglucinol in the interactions of the biocontrol pseudomonad F113 with the potato cyst nematode Globodera rostochiensis. Appl Environ Microbiol 63:1357–1361PubMedGoogle Scholar
  55. de Boer W, Wagenaar A-M, Klein Gunnewiek PJA, van Veen JA (2007) In vitro suppression of fungi caused by combinations of apparently non-antagonistic soil bacteria. FEMS Microbiol Ecol 59:177–185PubMedCrossRefGoogle Scholar
  56. De Marco J, Felix C (2002) Characterization of a protease produced by a Trichoderma harzianum isolate which controls cocoa plant witches’ broom disease. BMC Biochem 3:3PubMedCrossRefGoogle Scholar
  57. de Souza JT, Raaijmakers JM (2003) Polymorphisms within the prnD and pltC genes from pyrrolnitrin and pyoluteorin-producing Pseudomonas and Burkholderia spp. FEMS Microbiol Ecol 43:21–34PubMedCrossRefGoogle Scholar
  58. Deleu M, Razafindralambo H, Popineau Y, Jacques P, Thonart P, Paquot M (1999) Interfacial and emulsifying properties of lipopeptides from Bacillus subtilis. Colloids Surf A Physicochem Eng Aspects 152:3–10CrossRefGoogle Scholar
  59. Dicklow MB, Acosta N, Zuckerman BM (1993) A novel Streptomyces species for controlling plant-parasitic nematodes. J Chem Ecol 19:159–173CrossRefGoogle Scholar
  60. Djonovic S, Vittone G, Mendoza-Herrera A, Kenerley CM (2007) Enhanced biocontrol activity of Trichoderma virens transformants constitutively coexpressing β-1,3- and β-1,6-glucanase genes. Mol Plant Pathol 8:469–480PubMedCrossRefGoogle Scholar
  61. Dobbelaere S, Croonenborghs A, Thys A, Vande BA, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:153–162CrossRefGoogle Scholar
  62. Domínguez J, Negrín MA, Rodríguez CM (2001) Aggregate water-stability, particle-size and soil solution properties in conducive and suppressive soils to Fusarium wilt of banana from Canary Islands (Spain). Soil Biol Biochem 33:449–455CrossRefGoogle Scholar
  63. Domínguez J, Negrín MA, Rodríguez CM (2003) Evaluating soil sodium indices in soils of volcanic nature conducive or suppressive to Fusarium wilt of banana. Soil Biol Biochem 35:565–575CrossRefGoogle Scholar
  64. Donadio S, Monciardini P, Sosio M (2007) Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep 24:1073–1109PubMedCrossRefGoogle Scholar
  65. Dong Y-H, Xu J-L, Li X-Z, Zhang L-H (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci USA 97:3526–3531PubMedCrossRefGoogle Scholar
  66. Dong Y-H, Zhang XF, Xu JL, Zhang LH (2004) Insecticidal Bacillus thuringiensis silences Erwinia carotovora virulence by a new form of microbial antagonism, signal interference. Appl Environ Microbiol 70:954–960PubMedCrossRefGoogle Scholar
  67. Dubeikovsky AN, Mordukhova EA, Kochetkov V, Polikarpova FY, Boronin AM (1993) Growth promotion of blackcurrant softwood cuttings by recombinant strain Pseudomonas fluorescens BSP53a synthesizing an increased amount of indole-3-acetic acid. Soil Biol Biochem 25:1277–1281CrossRefGoogle Scholar
  68. Duffy BK, Ownley BH, Weller DM (1997) Soil chemical and physical properties associated with suppression of take-all of wheat by Trichoderma koningii. Phytopathology 87:1118–1124PubMedCrossRefGoogle Scholar
  69. Duijff BJ, Meijer JW, Bakker PAHM, Schippers B (1993) Siderophore-mediated competition for iron and induced resistance in the suppression of fusarium wilt of carnation by fluorescent Pseudomonas spp. Eur J Plant Pathol 99:277–289Google Scholar
  70. Dunne C, Crowley JJ, Moënne-Loccoz Y, Dowling DN, de Bruijn FJ, O’Gara F (1997) Biological control of Pythium ultimum by Stenotrophomonas maltophilia W81 is mediated by an extracellular proteolytic activity. Microbiology 143:3921–3931CrossRefGoogle Scholar
  71. Duponnois R, Mateille T, Gueye M (1995) Biological characteristics and effects of two strains of Arthrobotrys oligospora from Senegal on Meloidogyne species parasitizing tomato plants. Biocontrol Sci Technol 5:517–526CrossRefGoogle Scholar
  72. Duponnois R, Fargette M, Fould S, Thioulouse J, Davies KG (2000) Diversity of the bacterial hyperparasite Pasteuria penetrans in relation to root-knot nematodes (Meloidogyne spp.) control on Acacia holosericea. Nematology 2:435–442CrossRefGoogle Scholar
  73. Dutky EM, Sayre RM (1978) Some factors affecting infection of nematodes by bacterial spore parasite Bacillus penetrans. J Nematol 10:285–285Google Scholar
  74. Edel V, Steinberg C, Gautheron N, Recorbet G, Alabouvette C (2001) Genetic diversity of Fusarium oxysporum populations isolated from different soils in France. FEMS Microbiol Ecol 36:61–71PubMedCrossRefGoogle Scholar
  75. Elad Y, Kapat A (1999) The role of Trichoderma harzianum protease in the biocontrol of Botrytis cinerea. Eur J Plant Pathol 105:177–189CrossRefGoogle Scholar
  76. Elad Y, Kirshner B, Yehuda N, Sztejnberg A (1998) Management of powdery mildew and gray mold of cucumber by Trichoderma harzianum T39 and Ampelomyces quisqualis AQ10. BioControl 43:241–251CrossRefGoogle Scholar
  77. El-Banna N, Winkelmann G (1998) Pyrrolnitrin from Burkholderia cepacia: antibiotic activity against fungi and novel activities against streptomycetes. J Appl Microbiol 85:69–78PubMedCrossRefGoogle Scholar
  78. Ellis RJ, Timms-Wilson TM, Bailey MJ (2000) Identification of conserved traits in fluorescent pseudomonads with antifungal activity. Environ Microbiol 2:274–284PubMedCrossRefGoogle Scholar
  79. Eparvier A, Alabouvette C (1994) Use of ELISA and GUS-transformed strains to study competition between pathogenic and nonpathogenic Fusarium oxysporum for root colonization. Biocontrol Sci Technol 4:35–47CrossRefGoogle Scholar
  80. Estevez de Jensen C, Percich JA, Graham PH (2002) Integrated management strategies of bean root rot with Bacillus subtilis and Rhizobium in Minnesota. Field Crop Res 74:107–115CrossRefGoogle Scholar
  81. Etebarian HR (2006) Evaluation of Streptomyces strains for biological control of charcoal stem rot of melon caused by Macrophomina phaseolina. Plant Pathol J 5:83–87CrossRefGoogle Scholar
  82. Ezziyyani M, Requena ME, Egea-Gilabert C, Candela ME (2007) Biological control of Phytophthora root rot of pepper using Trichoderma harzianum and Streptomyces rochei in combination. J Phytopathol 155:342–349CrossRefGoogle Scholar
  83. Fang JG, Tsao PH (1994) Evaluation of Pythium nunn as a potential biocontrol agent against Phytophthora root rots of azalea and sweet orange. Phytopathology 85:29–36CrossRefGoogle Scholar
  84. Fenton AM, Stephens PM, Crowley J, O’Callaghan 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 58:3873–3878PubMedGoogle Scholar
  85. Frapolli M, Défago G, Moënne-Loccoz Y (2010) Denaturing gradient gel electrophoretic analysis of dominant 2,4-diacetylphloroglucinol biosynthetic phlD alleles in fluorescent Pseudomonas from soils suppressive or conducive to black root rot of tobacco. Soil Biol Biochem 42:649–656CrossRefGoogle Scholar
  86. Fravel D, Olivain C, Alabouvette C (2003) Fusarium oxysporum and its biocontrol. New Phytol 157:493–502CrossRefGoogle Scholar
  87. Fuchs JG, Moënne-Loccoz Y, Défago G (1997) Nonpathogenic Fusarium oxysporum strain Fo47 induces resistance to Fusarium wilt in tomato. Plant Dis 81:492–496CrossRefGoogle Scholar
  88. Garbeva P, Postma J, van Veen JA, van Elsas JD (2006) Effect of above-ground plant species on soil microbial community structure and its impact on suppression of Rhizoctonia solani AG3. Environ Microbiol 8:233–246PubMedCrossRefGoogle Scholar
  89. George E, Marschner H, Jakobsen I (1995) Role of arbuscular mycorrhizal fungi in uptake of phosphorus and nitrogen from soil. Crit Rev Biotechnol 15:257–270CrossRefGoogle Scholar
  90. Gerth K, Trowitzsch W, Wray V, Hofle G, Irschik H, Reichenbach H (1982) Pyrrolnitrin from Myxococcus fulvus (Myxobacterales). J Antibiot 35:1101–1103PubMedCrossRefGoogle Scholar
  91. Ghosh TK, Saha KC (1993) Effects of inoculation with N2-fixing cyanobacteria on the nitrogenase activity in soil and rhizosphere of wetland rice (Oryza sativa L.). Biol Fertil Soils 16:16–20CrossRefGoogle Scholar
  92. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7PubMedCrossRefGoogle Scholar
  93. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68PubMedCrossRefGoogle Scholar
  94. Goodridge LD (2004) Bacteriophage biocontrol of plant pathogens: fact or fiction? Trends Biotechnol 22:384–385PubMedCrossRefGoogle Scholar
  95. Griffiths B, Robinson D (1992) Root-induced nitrogen mineralisation: a nitrogen balance model. Plant Soil 139:253–263CrossRefGoogle Scholar
  96. Gupta VP, Tewari SK, Govindaiah BAK (1999) Ultrastructure of mycoparasitism of Trichoderma, Gliocladium and Laetisaria species on Botryodiplodia theobromae. J Phytopathol 147:19–24Google Scholar
  97. Gutierrez-Manero FJ, Ramos-Solano B, Probanza AN, Mehouachi J, R. Tadeo F, Talon M (2001) The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plant 111:206–211CrossRefGoogle Scholar
  98. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319PubMedCrossRefGoogle Scholar
  99. 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 41:117–153PubMedCrossRefGoogle Scholar
  100. Han JS, Cheng JH, Yoon TM, Song J, Rajkarnikar A, Kim WG, Yoo ID, Yang YY, Suh JW (2005a) Biological control agent of common scab disease by antagonistic strain Bacillus sp. sunhua. J Appl Microbiol 99:213–221PubMedCrossRefGoogle Scholar
  101. Han J, Sun L, Dong X, Cai Z, Sun X, Yang H, Wang Y, Song W (2005b) Characterization of a novel plant growth-promoting bacteria strain Delftia tsuruhatensis HR4 both as a diazotroph and a potential biocontrol agent against various plant pathogens. Syst Appl Microbiol 28:66–76PubMedCrossRefGoogle Scholar
  102. Helbig J (2001) Biological control of Botrytis cinerea Pers. ex Fr. in strawberry by Paenibacillus polymyxa (isolate 18191). J Phytopathol 149:265–273CrossRefGoogle Scholar
  103. Heulin T, Guckert A, Balandreau J (1987) Stimulation of root exudation of rice seedlings by Azospirillum strains: carbon budget under gnotobiotic conditions. Biol Fertil Soils 4:9–17Google Scholar
  104. Hiradate S, Yoshida S, Sugie H, Yada H, Fujii Y (2002) Mulberry anthracnose antagonists (iturins) produced by Bacillus amyloliquefaciens RC-2. Phytochemistry 61:693–698PubMedCrossRefGoogle Scholar
  105. Hjort K, Lembke A, Speksnijder A, Smalla K, Jansson JK (2007) Community structure of actively growing bacterial populations in plant pathogen suppressive soil. Microb Ecol 53:399–413PubMedCrossRefGoogle Scholar
  106. Hjort K, Bergström M, Adesina MF, Jansson JK, Smalla K, Sjöling S (2010) Chitinase genes revealed and compared in bacterial isolates, DNA extracts and a metagenomic library from a phytopathogen-suppressive soil. FEMS Microbiol Ecol 71:197–207PubMedCrossRefGoogle Scholar
  107. Hontzeas N, Richardson AO, Belimov A, Safronova V, Abu-Omar MM, Glick BR (2005) Evidence for horizontal transfer of 1-aminocyclopropane-1-carboxylate deaminase genes. Appl Environ Microbiol 71:7556–7558PubMedCrossRefGoogle Scholar
  108. Höper H, Steinberg C, Alabouvette C (1995) Involvement of clay type and pH in the mechanisms of soil suppressiveness to fusarium wilt of flax. Soil Biol Biochem 27:955–967CrossRefGoogle Scholar
  109. Hopwood DA (2003) Antibiotics actions, origins, resistance. Science 301:1850–1851CrossRefGoogle Scholar
  110. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10CrossRefGoogle Scholar
  111. Huang X, Tian B, Niu Q, Yang J, Zhang L, Zhang K (2005) An extracellular protease from Brevibacillus laterosporus G4 without parasporal crystals can serve as a pathogenic factor in infection of nematodes. Res Microbiol 156:719–727PubMedCrossRefGoogle Scholar
  112. Hwang J, Benson DM (2002) Biocontrol of Rhizoctonia stem and root rot of Poinsettia with Burkholderia cepacia and binucleate Rhizoctonia. Plant Dis 86:47–53CrossRefGoogle Scholar
  113. Hwang J, Benson DM (2003) Expression of induced systemic resistance in poinsettia cuttings against Rhizoctonia stem rot by treatment of stock plants with binucleate Rhizoctonia. Biol Control 27:73–80CrossRefGoogle Scholar
  114. Iavicoli A, Boutet E, Buchala A, Métraux JP (2003) Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol Plant-Microbe Interact 16:851–858PubMedCrossRefGoogle Scholar
  115. Islam MT, Hashidoko Y, Deora A, Ito T, Tahara S (2005) Suppression of damping-off disease in host plants by the rhizoplane bacterium Lysobacter sp. strain SB-K88 is linked to plant colonization and antibiosis against soilborne peronosporomycetes. Appl Environ Microbiol 71:3786–3796PubMedCrossRefGoogle Scholar
  116. Jager G, Velvis H (1986) Biological control of Rhizoctonia solani on potatoes by antagonists. 5. The effectiveness of three isolates of Verticillium biguttatum as inoculum for seed tubers and of a soil treatment with a low dosage of pencycuron. Neth J Plant Pathol 92:231–238CrossRefGoogle Scholar
  117. Jakobi M, Winkelmann G, Kaiser D, Kempter C, Jung G, Berg G, Bahl H (1996) Maltophilin: a new antifungal compound produced by Stenotrophomonas maltophilia R3089. J Antibiot 49:1101–1104PubMedCrossRefGoogle Scholar
  118. Janvier C, Villeneuve F, Alabouvette C, Edel-Hermann V, Mateille T, Steinberg C (2007) Soil health through soil disease suppression: which strategy from descriptors ? Soil Biol Biochem 39:1–23CrossRefGoogle Scholar
  119. John UP, Nagley P (1986) Aminoacid substitutions in mitochondrial ATPase subunit-6 of Saccharomyces cerevisiae leading to oligomycin resistance. FEBS Lett 207:79–83PubMedCrossRefGoogle Scholar
  120. Johnsen K, Enger O, Jacobsen CS, Thirup L, Torsvik V (1999) Quantitative selective PCR of 16S ribosomal DNA correlates well with selective agar plating in describing population dynamics of indigenous Pseudomonas spp. in soil hot spots. Appl Environ Microbiol 65:1786–1788PubMedGoogle Scholar
  121. Jorgenson EC (1970) Antagonistic interaction of Heterodera schachtii Schmidt and Fusarium oxysporum (Woll.) on sugarbeets. J Nematol 2:393–398PubMedGoogle Scholar
  122. Kajimura Y, Kaneda M (1996) Fusaricidin A, a new depsipeptide antibiotic produced by Bacillus polymyxa KT-8 – taxonomy, fermentation, isolation, structure elucidation and biological activity. J Antibiot 49:129–135PubMedCrossRefGoogle Scholar
  123. Kalbe C, Marten P, Berg G (1996) Strains of the genus Serratia as beneficial rhizobacteria of oilseed rape with antifungal properties. Microbiol Res 151:433–439PubMedCrossRefGoogle Scholar
  124. Kamensky M, Ovadis M, Chet I, Chernin L (2003) Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol Biochem 35:323–331CrossRefGoogle Scholar
  125. Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B (2005) Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7:1809–1817PubMedCrossRefGoogle Scholar
  126. Kamilova K, Leveau JHJ, Lugtenberg B (2007) Collimonas fungivorans, an unpredicted in vitro but efficient in vivo biocontrol agent for the suppression of tomato foot and root rot. Environ Microbiol 9:1597–1603PubMedCrossRefGoogle Scholar
  127. 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 64:3939–3947PubMedGoogle Scholar
  128. Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger U, Wirthner P, Haas D, Défago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHA0 – importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol Plant-Microbe Interact 5:4–13CrossRefGoogle Scholar
  129. Kennedy IR, Choudhury ATMA, Kecskes ML (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biol Biochem 36:1229–1244CrossRefGoogle Scholar
  130. Kerry BR (1982) The decline of Heterodera avenae populations. EPPO Bull 12:491–496CrossRefGoogle Scholar
  131. Khan NI, Filonow AB, Singleton LL (1997) Augmentation of soil with sporangia of Actinoplanes spp. for biological control of Pythium damping-off. Biocontrol Sci Technol 7:11–22CrossRefGoogle Scholar
  132. Kilic-Ekici O, Yuen GY (2003) Induced resistance as a mechanism of biological control by Lysobacter enzymogenes strain C3. Phytopathology 93:1103–1110PubMedCrossRefGoogle Scholar
  133. Kim B, Moon SS, Hwang BK (1999) Isolation, identification, and antifungal activity of a macrolide antibiotic, oligomycin A, produced by Streptomyces libani. Can J Bot 77:850–858Google Scholar
  134. Kinkel LL, Bowers JH, Shimizu K, Neeno-Eckwall EC, Schottel JL (1998) Quantitative relationships among thaxtomin A production, potato scab severity, and fatty acid composition in Streptomyces. Can J Microbiol 44:768–776PubMedGoogle Scholar
  135. Kishore GK, Pande S, Podile AR (2005) Biological control of late leaf spot of peanut (Arachis hypogaea) with chitinolytic bacteria. Phytopathology 95:1157–1165PubMedCrossRefGoogle Scholar
  136. Kobayashi DY, Guglielmoni M, Clarke BB (1995) Isolation of the chitinolytic bacteria Xanthomonas maltophilia and Serratia marcescens as biological control agents for summer patch disease of turfgrass. Soil Biol Biochem 27:1479–1487CrossRefGoogle Scholar
  137. Kobayashi DY, Reedy RM, Bick J, Oudemans PV (2002) Characterization of a chitinase gene from Stenotrophomonas maltophilia strain 34S1 and its involvement in biological control. Appl Environ Microbiol 68:1047–1054PubMedCrossRefGoogle Scholar
  138. Kyselková M, Kopecký J, Frapolli M, Défago G, Ságová-Marečková M, Grundmann GL, Moënne-Loccoz Y (2009) Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. ISME J 3:1127–1138PubMedCrossRefGoogle Scholar
  139. 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 68:3226–3237PubMedCrossRefGoogle Scholar
  140. Landa BB, Mavrodi OV, Schroeder KL, Allende-Molar R, Weller DM (2006) Enrichment and genotypic diversity of phlD-containing fluorescent Pseudomonas spp. in two soils after a century of wheat and flax monoculture. FEMS Microbiol Ecol 55:351–368PubMedCrossRefGoogle Scholar
  141. Larcher M, Muller B, Mantelin S, Rapior S, Cleyet-Marel JC (2003) Early modifications of Brassica napus root system architecture induced by a plant growth-promoting Phyllobacterium strain. New Phytol 160:119–125CrossRefGoogle Scholar
  142. Larkin RP, Fravel DR (1998) Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Phytopathology 88:1022–1028Google Scholar
  143. Larkin RP, Fravel DR (1999) Mechanisms of action and dose-response relationships governing biological control of fusarium wilt of tomato by nonpathogenic Fusarium spp. Phytopathology 89:1152–1161PubMedCrossRefGoogle Scholar
  144. Larkin RP, Hopkins DL, Martin FN (1996) Suppression of Fusarium wilt of watermelon by nonpathogenic Fusarium oxysporum and other microorganisms recovered from a disease-suppressive soil. Phytopathology 86:812–819CrossRefGoogle Scholar
  145. Lebreton L, Lucas P, Dugas F, Guillerm AY, Schoeny A, Sarniguet A (2004) Changes in population structure of the soilborne fungus Gaeumannomyces graminis var. tritici during continuous wheat cropping. Environ Microbiol 6:1174–1185PubMedCrossRefGoogle Scholar
  146. Lee HB, Kim Y, Kim JC, Choi GJ, Park SH, Kim CJ, Jung HS (2005) Activity of some aminoglycoside antibiotics against true fungi, Phytophthora and Pythium species. J Appl Microbiol 99:836–843PubMedCrossRefGoogle Scholar
  147. Leelasuphakul W, Sivanunsakul P, Phongpaichit S (2006) Purification, characterization and synergistic activity of β-1,3-glucanase and antibiotic extract from an antagonistic Bacillus subtilis NSRS 89-24 against rice blast and sheath blight. Enzyme Microb Technol 38:990–997CrossRefGoogle Scholar
  148. Lemanceau P, Alabouvette C (1991) Biological control of fusarium diseases by fluorescent pseudomonas and nonpathogenic Fusarium. Crop Prot 10:279–286CrossRefGoogle Scholar
  149. Lemanceau P, Alabouvette C (1993) Suppression of Fusarium wilt by fluorescent pseudomonads – mechanisms and applications. Biocontrol Sci Tech 3:219–234CrossRefGoogle Scholar
  150. Lemanceau P, Bakker PAHM, De Kogel WJ, Alabouvette C, Schippers B (1992) Effect of pseudobactin 358 production by Pseudomonas putida WCS358 on suppression of Fusarium wilt of carnations by nonpathogenic Fusarium oxysporum Fo47. Appl Environ Microbiol 58:2978–2982PubMedGoogle Scholar
  151. Lemanceau P, Bakker PAHM, De Kogel WJ, Alabouvette C, Schippers B (1993) Antagonistic effect of nonpathogenic Fusarium oxysporum Fo47 and pseudobactin 358 upon pathogenic Fusarium oxysporum f. sp. dianthi. Appl Environ Microbiol 59:74–82PubMedGoogle Scholar
  152. Lemanceau P, Maurhofer M, Défago G (2006) Contribution of studies on suppressive soils to the identification of bacterial biocontrol agents and to the knowledge of their modes of action. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 231–267CrossRefGoogle Scholar
  153. Li W, Roberts DP, Dery PD, Meyer SLF, Lohrke S, Lumsden RD, Hebbar KP (2002) Broad spectrum antibiotic activity and disease suppression by the potential biocontrol agent Burkholderia ambifaria BC-F. Crop Prot 21:129–135CrossRefGoogle Scholar
  154. Li GQ, Huang HC, Acharya SN, Erickson RS (2005) Effectiveness of Coniothyrium minitans and Trichoderma atroviride in suppression of sclerotinia blossom blight of alfalfa. Plant Pathol 54:204–211CrossRefGoogle Scholar
  155. 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 98:695–701PubMedCrossRefGoogle Scholar
  156. Lian LH, Tian BY, Xiong R, Zhu MZ, Xu J, Zhang KQ (2007) Proteases from Bacillus: a new insight into the mechanism of action for rhizobacterial suppression of nematode populations. Lett Appl Microbiol 45:262–269PubMedCrossRefGoogle Scholar
  157. Lifshitz R, Dupler M, Elad Y, Baker R (1984) Hyphal interactions between a mycoparasite, Pythium nunn, and several soil fungi. Can J Microbiol 30:1482–1487CrossRefGoogle Scholar
  158. Lim H-S, Kim Y-S, Kim S-D (1991) Pseudomonas stutzeri YPL-1 genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot. Appl Environ Microbiol 57:510–516PubMedGoogle Scholar
  159. Lippmann B, Leinhos V, Bergmann H (1995) Influence of auxin producing rhizobacteria on root morphology and nutrient accumulation of crops. I. Changes in root morphology and nutrient accumulation in maize (Zea mays L.) caused by inoculation with indole-3-acetic acid (IAA) producing Pseudomonas and Acinetobacter strains or IAA applied exogenously. Angew Bot 69:31–36Google Scholar
  160. Liu DQ, Anderson NA, Kinkel LL (1995) Biological control of potato scab in the field with antagonistic Streptomyces scabies. Phytopathology 85:827–831CrossRefGoogle Scholar
  161. Loper JE, Ishimaru CA, Carnegie SR, Vanavichit A (1993) Cloning and characterization of aerobactin biosynthesis genes of the biological control agent Enterobacter cloacae. Appl Environ Microbiol 59:4189–4197PubMedGoogle Scholar
  162. Lorang JM, Liu D, Anderson NA, Schottel JL (1995) Identification of potato scab inducing and suppressive species of Streptomyces. Phytopathology 85:261–268CrossRefGoogle Scholar
  163. Lumsden RD, Locke JC, Adkins ST, Walter JF, Ridout CJ (1992) Isolation and localization of the antibiotic gliotoxin produced by Gliocladium virens from alginate prill in soil and soilless media. Phytopathology 82:230–235CrossRefGoogle Scholar
  164. Lutz MP, Wenger S, Maurhofer M, Défago G, Duffy B (2004) Signaling between bacterial and fungal biocontrol agents in a strain mixture. FEMS Microbiol Ecol 48:447–455PubMedCrossRefGoogle Scholar
  165. 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 56:167–177PubMedCrossRefGoogle Scholar
  166. Mateille T, Cadet P, Fargette M (2008) Control and management of plant-parasitic nematode communities in a soil conservation approach. In: Ciancio A, Mukerji KG (eds) Integrated management and biocontrol of vegetable and grain crops nematodes. Springer, Dordrecht, pp 79–97Google Scholar
  167. Mathre DE, Johnston RH, Grey WE (1998) Biological control of take-all disease of wheat caused by Gaeumannomyces graminis var. tritici under field conditions using a Phialophora sp. Biocontrol Sci Technol 8:449–457CrossRefGoogle Scholar
  168. Maurhofer M, Keel C, Haas D, Défago G (1994) Pyoluteorin production by Pseudomonas fluorescens strain CHA0 is involved in the suppression of Pythium damping-off of cress but not of cucumber. Eur J Plant Pathol 100:221–232CrossRefGoogle Scholar
  169. Mazurier S, Lemunier M, Siblot S, Mougel C, Lemanceau P (2004) Distribution and diversity of type III secretion system-like genes in saprophytic and phytopathogenic fluorescent pseudomonads. FEMS Microbiol Ecol 49:455–467PubMedCrossRefGoogle Scholar
  170. 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 3:977–991PubMedCrossRefGoogle Scholar
  171. Mazzola M (2002) Mechanisms of natural soil suppressiveness to soilborne diseases. Anton Leeuw 81:557–564CrossRefGoogle Scholar
  172. Mazzola M, Gu YH (2000) Impact of wheat cultivation on microbial communities from replant soils and apple growth in greenhouse trials. Phytopathology 90:114–119PubMedCrossRefGoogle Scholar
  173. 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 58:2616–2624PubMedGoogle Scholar
  174. Mazzola M, Fujimoto DK, Thomashow LS, Cook RJ (1995) Variation in sensitivity of Gaeumannomyces graminis to antibiotics produced by fluorescent Pseudomonas spp. and effect on biological control of take-all of wheat. Appl Environ Microbiol 61:2554–2559PubMedGoogle Scholar
  175. McSpadden Gardener BB, Weller DM (2001) Changes in populations of rhizosphere bacteria associated with take-all disease of wheat. Appl Environ Microbiol 67:4414–4425PubMedCrossRefGoogle Scholar
  176. Medina-Martinez MS, Uyttendaele M, Rajkovic A, Nadal P, Debevere J (2007) Degradation of N-acyl-L-homoserine lactones by Bacillus cereus in culture media and pork extract. Appl Environ Microbiol 73:2329–2332PubMedCrossRefGoogle Scholar
  177. Meera MS, Shivanna MB, Kageyama K, Hyakumachi M (1995) Responses of cucumber cultivars to induction of systemic resistance against anthracnose by plant growth promoting fungi. Eur J Plant Pathol 101:421–430CrossRefGoogle Scholar
  178. Messiha N, van Diepeningen A, Farag N, Abdallah S, Janse J, van Bruggen A (2007) Stenotrophomonas maltophilia: a new potential biocontrol agent of Ralstonia solanacearum, causal agent of potato brown rot. Eur J Plant Pathol 118:211–225CrossRefGoogle Scholar
  179. Metcalf DA, Wilson CR (2001) The process of antagonism of Sclerotium cepivorum in white rot affected onion roots by Trichoderma koningii. Plant Pathol 50:249–257CrossRefGoogle Scholar
  180. Milner JL, SiloSuh L, Lee JC, He HY, Clardy J, Handelsman J (1996) Production of kanosamine by Bacillus cereus UW85. Appl Environ Microbiol 62:3061–3065PubMedGoogle Scholar
  181. Minerdi D, Moretti M, Gilardi G, Barberio C, Gullino ML, Garibaldi A (2008) Bacterial ectosymbionts and virulence silencing in a Fusarium oxysporum strain. Environ Microbiol 10:1725–1741PubMedCrossRefGoogle Scholar
  182. Minerdi D, Bossi S, Gullino ML, Garibaldi A (2009) Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol 11:844–854PubMedCrossRefGoogle Scholar
  183. Mirza MS, Mehnaz S, Normand P, Prigent-Combaret C, Moënne-Loccoz Y, Bally R, Malik KA (2006) Molecular characterization and PCR detection of a nitrogen-fixing Pseudomonas strain promoting rice growth. Biol Fertil Soils 43:163–170CrossRefGoogle Scholar
  184. Moënne-Loccoz Y, McHugh B, Stephens PM, McConnell FI, Glennon JD, Dowling DN, O’Gara F (1996) Rhizosphere competence of fluorescent Pseudomonas sp. B24 genetically modified to utilise additional ferric siderophores. FEMS Microbiol Ecol 19:215–225CrossRefGoogle Scholar
  185. Moënne-Loccoz Y, Tichy HV, O’Donnell A, Simon R, O’Gara F (2001) Impact of 2,4-diacetylphloroglucinol-producing biocontrol strain Pseudomonas fluorescens F113 on intraspecific diversity of resident culturable fluorescent pseudomonads associated with the roots of field-grown sugar beet seedlings. Appl Environ Microbiol 67:3418–3425PubMedCrossRefGoogle Scholar
  186. Murakami H, Tsushima S, Shishido Y (2000) Soil suppressiveness to clubroot disease of Chinese cabbage caused by Plasmodiophora brassicae. Soil Biol Biochem 32:1637–1642CrossRefGoogle Scholar
  187. Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen-fixation. Plant Cell 7:869–885PubMedCrossRefGoogle Scholar
  188. Natsch A, Keel C, Hebecker N, Laasik E, Défago G (1998) Impact of Pseudomonas fluorescens strain CHA0 and a derivative with improved biocontrol activity on the culturable resident bacterial community on cucumber roots. FEMS Microbiol Ecol 27:365–380CrossRefGoogle Scholar
  189. Neeno-Eckwall EC, Kinkel LL, Schottel JL (2001) Competition and antibiosis in the biological control of potato scab. Can J Microbiol 47:332–340PubMedCrossRefGoogle Scholar
  190. Neilands JB (1995) Siderophores – structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726PubMedGoogle Scholar
  191. Neipp PW, Becker JO (1999) Evaluation of biocontrol activity of rhizobacteria from Beta vulgaris against Heterodera schachtii. J Nematol 31:54–61PubMedGoogle Scholar
  192. Oberhansli T, Défago G, Haas D (1991) Indole-3-acetic acid (IAA) synthesis in the biocontrol strain CHA0 of Pseudomonas fluorescens: role of tryptophan side chain oxidase. J Gen Microbiol 137:2273–2279PubMedGoogle Scholar
  193. Olatinwo R, Yin B, Becker JO, Borneman J (2006) Suppression of the plant-parasitic nematode Heterodera schachtii by the fungus Dactylella oviparasitica. Phytopathology 96:111–114PubMedCrossRefGoogle Scholar
  194. Omarjee J, Balandreau J, Spaull VW, Cadet P (2008) Relationships between Burkholderia populations and plant parasitic nematodes in sugarcane. Appl Soil Ecol 39:1–14CrossRefGoogle Scholar
  195. Ongena M, Jourdan E, Adam A, Schäfer M, Budzikiewicz H, Thonart P (2007) Amino acids, iron, and growth rate as key factors influencing production of the Pseudomonas putida BTP1 benzylamine derivative involved in systemic resistance induction in different plants. Microbiol Ecol 55:280–292CrossRefGoogle Scholar
  196. Palumbo JD, Yuen GY, Jochum CC, Tatum K, Kobayashi DY (2005) Mutagenesis of β-1,3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward bipolaris leaf spot of tall fescue and Pythium damping-off of sugar beet. Phytopathology 95:701–707PubMedCrossRefGoogle Scholar
  197. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801PubMedCrossRefGoogle Scholar
  198. Paulitz TC, Anas O, Fernando DG (1992) Biological control of Pythium damping-off by seed treatment with Pseudomonas putida – relationship with ethanol production by pea and soybean seeds. Biocontrol Sci Technol 2:193–201CrossRefGoogle Scholar
  199. Peix A, Rivas R, Mateos PF, Martínez-Molina E, Rodríguez-Barrueco C, Velásquez E (2003) Pseudomonas rhizosphaerae sp. nov., a novel species that actively solubilizes phosphate in vitro. Int J Syst Evol Microbiol 53:2067–2072PubMedCrossRefGoogle Scholar
  200. Persson L, Larsson-Wikstrom M, Gerhardson B (1999) Assessment of soil suppressiveness to Aphanomyces root rot of pea. Plant Dis 83:1108–1112CrossRefGoogle Scholar
  201. Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136:2887–2894PubMedCrossRefGoogle Scholar
  202. Picard C, Frascaroli E, Bosco M (2004) Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing rhizobacteria are differentially affected by the genotype of two maize inbred lines and their hybrid. FEMS Microbiol Ecol 49:207–215PubMedCrossRefGoogle Scholar
  203. Pichard B, Larue JP, Thouvenot D (1995) Gavaserin and saltavalin, new peptide antibiotics produced by Bacillus polymyxa. FEMS Microbiol Lett 133:215–218PubMedCrossRefGoogle Scholar
  204. Pieterse CMJ, van Pelt JA, Verhagen BWM, Ton J, van Wees SCM, Leon-Kloosterziel KM, van Loon LC (2003) Induced systemic resistance by plant growth-promoting rhizobacteria. Symbiosis 35:39–54Google Scholar
  205. Pinon D, Casas M, Blanch M, Fontaniella B, Blanco Y, Vicente C, Solas MT, Legaz ME (2002) Gluconacetobacter diazotrophicus, a sugar cane endosymbiont, produces a bacteriocin against Xanthomonas albilineans, a sugar cane pathogen. Res Microbiol 153:345–351PubMedCrossRefGoogle Scholar
  206. Postma J, Scheper RWA, Schilder MT (2010) Effect of successive cauliflower plantings and Rhizoctonia solani AG 2-1 inoculations on disease suppressiveness of a suppressive and a conducive soil. Soil Biol Biochem 42:804–812CrossRefGoogle Scholar
  207. Press CM, Wilson M, Tuzun S, Kloepper JW (1997) Salicylic acid produced by Serratia marcescens 90-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol Plant-Microbe Interact 10:761–768CrossRefGoogle Scholar
  208. Preston GM, Bertrand N, Rainey PB (2001) Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25. Mol Microbiol 41:999–1014PubMedCrossRefGoogle Scholar
  209. Raaijmakers JM, Weller DM (1998) Natural plant protection by 2,4-diacetylphloroglucinol producing Pseudomonas spp. in take-all decline soils. Mol Plant-Microbe Interact 11:144CrossRefGoogle Scholar
  210. 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 89:470–475PubMedCrossRefGoogle Scholar
  211. Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Anton Leeuw 81:537–547CrossRefGoogle Scholar
  212. Raaijmakers JM, Paulitz TC, Alabouvette C, Steinberg C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361CrossRefGoogle Scholar
  213. Ramette A, Moënne-Loccoz Y, Défago G (2001) Polymorphism of the polyketide synthase gene phlD in biocontrol fluorescent pseudomonads producing 2,4-diacetylphloroglucinol and comparison of PhlD with plant polyketide synthases. Mol Plant-Microbe Interact 14:639–652PubMedCrossRefGoogle Scholar
  214. Ramette A, Frapolli M, Défago G, Moënne-Loccoz Y (2003a) Phylogeny of HCN synthase-encoding hcnBC genes in biocontrol fluorescent pseudomonads and its relationship with host plant species and HCN synthesis ability. Mol Plant-Microbe Interact 16:525–535PubMedCrossRefGoogle Scholar
  215. Ramette A, Moënne-Loccoz Y, Défago G (2003b) Prevalence of fluorescent pseudomonads producing antifungal phloroglucinols and/or hydrogen cyanide in soils naturally suppressive or conducive to tobacco black root rot. FEMS Microbiol Ecol 44:35–43PubMedCrossRefGoogle Scholar
  216. Ramette A, Moënne-Loccoz Y, Défago G (2006) Genetic diversity and biocontrol potential of fluorescent pseudomonads producing phloroglucinols and hydrogen cyanide from Swiss soils naturally suppressive or conducive to Thielaviopsis basicola-mediated black root rot of tobacco. FEMS Microbiol Ecol 55:369–381PubMedCrossRefGoogle Scholar
  217. Ramette A, Frapolli M, Fischer-Le Saux M, Gruffaz C, Meyer JM, Défago G, Sutra L, Moënne-Loccoz Y (2011) Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin. Syst Appl Microbiol 34:180–188PubMedCrossRefGoogle Scholar
  218. Ramos B, Lucas García JA, Probanza A, Barrientos ML, Gutierrez Mañero FJ (2003) Alterations in the rhizobacterial community associated with European alder growth when inoculated with PGPR strain Bacillus licheniformis. Environ Exp Bot 49:61–68CrossRefGoogle Scholar
  219. Recht MI, Douthwaite S, Puglisi JD (1999) Basis for prokaryotic specificity of action of aminoglycoside antibiotics. EMBO J 18:3133–3138PubMedCrossRefGoogle Scholar
  220. Reichenbach H (2001) Myxobacteria, producers of novel bioactive substances. J Ind Microbiol Biotechnol 27:149–156PubMedCrossRefGoogle Scholar
  221. Rezzonico F, Défago G, Moënne-Loccoz Y (2004) Comparison of ATPase-encoding type III secretion system hrcN genes in biocontrol fluorescent pseudomonads and in phytopathogenic proteobacteria. Appl Environ Microbiol 70:5119–5131PubMedCrossRefGoogle Scholar
  222. Rezzonico F, Binder C, Défago G, Moënne-Loccoz Y (2005) The type III secretion system of biocontrol Pseudomonas fluorescens KD targets the phytopathogenic Chromista Pythium ultimum and promotes cucumber protection. Mol Plant-Microbe Interact 18:991–1001PubMedCrossRefGoogle Scholar
  223. Rezzonico F, Zala M, Keel C, Duffy B, Moënne-Loccoz Y, Défago G (2007) Is the ability of biocontrol fluorescent pseudomonads to produce the antifungal metabolite 2,4-diacetylphloroglucinol really synonymous with higher plant protection? New Phytol 173:861–872PubMedCrossRefGoogle Scholar
  224. Rimé D, Nazaret S, Gourbière F, Cadet P, Moënne-Loccoz Y (2003) Comparison of sandy soils suppressive or conducive to ectoparasitic nematode damage on sugarcane. Phytopathology 93:1437–1444PubMedCrossRefGoogle Scholar
  225. Roberts DP, McKenna LF, Lakshman DK, Meyer SLF, Kong H, de Souza JT, Lydon J, Baker CJ, Buyer JS, Chung S (2007) Suppression of damping-off of cucumber caused by Pythium ultimum with live cells and extracts of Serratia marcescens N4-5. Soil Biol Biochem 39:2275–2288CrossRefGoogle Scholar
  226. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339PubMedCrossRefGoogle Scholar
  227. Roget DK (1995) Decline in root rot (Rhizoctonia solani AG-8) in wheat in a tillage and rotation experiment at Avon, South Australia. Aust J Exp Agric 35:1009–1013CrossRefGoogle Scholar
  228. Russo A, Vettori L, Felici C, Fiaschi G, Morini S, Toffanin A (2008) Enhanced micropropagation response and biocontrol effect of Azospirillum brasilense Sp245 on Prunus cerasifera L. clone Mr.S 2/5 plants. J Biotechnol 134:312–319PubMedCrossRefGoogle Scholar
  229. Ryu C-M, Kim J, Choi O, Kim SH, Park CS (2006) Improvement of biological control capacity of Paenibacillus polymyxa E681 by seed pelleting on sesame. Biol Control 39:282–289CrossRefGoogle Scholar
  230. Sabaratnam S, Traquair JA (2002) Formulation of a Streptomyces biocontrol agent for the suppression of Rhizoctonia damping-off in tomato transplants. Biol Control 23:245–253CrossRefGoogle Scholar
  231. Sadowsky MJ, Kinkel LL, Bowers JH, Schottel JL (1996) Use of repetitive intergenic DNA sequences to classify pathogenic and disease-suppressive Streptomyces strains. Appl Environ Microbiol 62:3489–3493PubMedGoogle Scholar
  232. Samac DA, Kinkel LL (2001) Suppression of the root-lesion nematode (Pratylenchus penetrans) in alfalfa (Medicago sativa) by Streptomyces spp. Plant Soil 235:35–44CrossRefGoogle Scholar
  233. Sanguin H, Kroneisen L, Gazengel K, Kyselková M, Remenant B, Prigent-Combaret C, Grundmann GL, Sarniguet A, Moënne-Loccoz Y (2008) Development of a 16S rRNA microarray approach for the monitoring of rhizosphere Pseudomonas populations associated with the decline of take-all disease of wheat. Soil Biol Biochem 40:1028–1039CrossRefGoogle Scholar
  234. Sanguin H, Sarniguet A, Gazengel K, Moënne-Loccoz Y, Grundmann GL (2009) Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. New Phytol 184:694–707PubMedCrossRefGoogle Scholar
  235. Sarniguet A, Lucas P (1992) Evaluation of populations of fluorescent pseudomonads related to decline of take-all patch on turfgrass. Plant Soil 145:11–15CrossRefGoogle Scholar
  236. Sayeed AM, Siddiqui ZA (2008) Glomus intraradices, Pseudomonas alcaligenes, and Bacillus pumilus: effective agents for the control of root-rot disease complex of chickpea (Cicer arietinum L.). J Gen Plant Pathol 74:53–60CrossRefGoogle Scholar
  237. Sayre RM, Wergin WP (1977) Bacterial parasite of a plant nematode – morphology and ultrastructure. J Bacteriol 129:1091–1101PubMedGoogle Scholar
  238. Scher FM, Baker R (1982) Effect of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness to Fusarium wilt pathogens. Phytopathology 72:1567–1573CrossRefGoogle Scholar
  239. Schippers B, Bakker AW, Bakker PAHM, van Peer R (1990) Beneficial and deleterious effects of HCN-producing pseudomonads on rhizosphere interactions. Plant Soil 129:75–83CrossRefGoogle Scholar
  240. Schlatter D, Fubuh A, Xiao K, Hernandez D, Hobbie S, Kinkel L (2009) Resource amendments influence density and competitive phenotypes of Streptomyces in soil. Microb Ecol 57:413–420PubMedCrossRefGoogle Scholar
  241. Schottel JL, Shimizu K, Kinkel LL (2001) Relationships of in vitro pathogen inhibition and soil colonization to potato scab biocontrol by antagonistic Streptomyces spp. Biol Control 20:102–112CrossRefGoogle Scholar
  242. Schouten A, Maksimova O, Cuesta-Arenas Y, van den Berg G, Raaijmakers JM (2008) Involvement of the ABC transporter BcAtrB and the laccase BcLCC2 in defence of Botrytis cinerea against the broad-spectrum antibiotic 2,4-diacetylphloroglucinol. Environ Microbiol 10:1145–1157PubMedCrossRefGoogle Scholar
  243. Schreiner K, Hagn A, Kyselková M, Moënne-Loccoz Y, Munch JC, Schloter M (2010) Comparison of barley succession and take-all disease as environmental factors shaping the rhizobacterial community during take-all decline. Appl Environ Microbiol 76:4703–4712PubMedCrossRefGoogle Scholar
  244. Shah S, Li JP, Moffatt BA, Glick BR (1998) Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. Can J Microbiol 44:833–843PubMedCrossRefGoogle Scholar
  245. Sharga BM, Lyon GD (1998) Bacillus subtilis BS 107 as an antagonist of potato blackleg and soft rot bacteria. Can J Microbiol 44:777–783PubMedGoogle Scholar
  246. 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 104:631–643CrossRefGoogle Scholar
  247. Sharon E, Bar-Eyal M, Chet I, Herrera-Estrella A, Kleifeld O, Spiegel Y (2001) Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology 91:687–693PubMedCrossRefGoogle Scholar
  248. Shen SS, Piao FZ, Lee BW, Park CS (2007) Characterization of antibiotic substance produced by Serratia plymuthica A21-4 and the biological control activity against pepper Phytophthora blight. Plant Pathol J 23:180–186CrossRefGoogle Scholar
  249. Shiomi Y, Nishiyama M, Onizuka T, Marumoto T (1999) Comparison of bacterial community structures in the rhizoplane of tomato plants grown in soils suppressive and conducive towards bacterial wilt. Appl Environ Microbiol 65:3996–4001PubMedGoogle Scholar
  250. Siddiqui IA, Ehteshamul-Haque S (2001) Suppression of the root rot–root knot disease complex by Pseudomonas aeruginosa in tomato: The influence of inoculum density, nematode populations, moisture and other plant-associated bacteria. Plant Soil 237:81–89CrossRefGoogle Scholar
  251. Siddiqui ZA, Mahmood I (1999) Role of bacteria in the management of plant parasitic nematodes: a review. Bioresour Technol 69:167–179CrossRefGoogle Scholar
  252. Silo-Suh LA, Lethbridge BJ, Raffel SJ, He HY, Clardy J, Handelsman J (1994) Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl Environ Microbiol 60:2023–2030PubMedGoogle Scholar
  253. Simon A, Sivasithamparam K (1989) Pathogen suppression – a case study in biological suppression of Gaeumannomyces graminis var. tritici in soil. Soil Biol Biochem 21:331–337CrossRefGoogle Scholar
  254. Smiley RW (1979) Wheat-rhizoplane pseudomonads as antagonists of Gaeumannomyces graminis. Soil Biol Biochem 11:371–376CrossRefGoogle Scholar
  255. Smith J, Putnam A, Nair M (1990) In vitro control of Fusarium diseases of Asparagus officinalis L. with a Streptomyces or its polyene antibiotic, faeriefungin. J Agric Food Chem 38:1729–1733CrossRefGoogle Scholar
  256. Somers E, Ptacek D, Gysegom P, Srinivasan M, Vanderleyden J (2005) Azospirillum brasilense produces the auxin-like phenylacetic acid by using the key enzyme for indole-3-acetic acid biosynthesis. Appl Environ Microbiol 71:1803–1810PubMedCrossRefGoogle Scholar
  257. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448PubMedCrossRefGoogle Scholar
  258. Spaull VW, Cadet P (1990) Nematodes parasites of sugarcane. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, pp 461–491Google Scholar
  259. Stabb EV, Jacobson LM, Handelsman J (1994) Zwittermicin A-producing strains of Bacillus cereus from diverse soils. Appl Environ Microbiol 60:4404–4412PubMedGoogle Scholar
  260. Steinberg C, Edel V, Gautheron N, Abadie C, Vallaeys T, Alabouvette C (1997) Phenotypic characterization of natural populations of Fusarium oxysporum in relation to genotypic characterization. FEMS Microbiol Ecol 24:73–85CrossRefGoogle Scholar
  261. Stipanovic RD, Howell CR (1982) The structure of gliovirin, a new antibiotic from Gliocladium virens. J Antibiot 35:1326–1330PubMedCrossRefGoogle Scholar
  262. Stirling GR, Mankau R (1979) Mode of parasitism of Meloidogyne and other nematode eggs by Dactylella oviparasitica. J Nematol 11:282–288PubMedGoogle Scholar
  263. Stockwell VO, Johnson KB, Sugar D, Loper JE (2002) Antibiosis contributes to biological control of fire blight by Pantoea agglomerans strain Eh252 in orchards. Phytopathology 92:1202–1209PubMedCrossRefGoogle Scholar
  264. Stotzky G, Martin RT (1963) Soil mineralogy in relation to the spread of Fusarium wilt of banana in Central America. Plant Soil 18:317–337CrossRefGoogle Scholar
  265. Stutz E, Défago G, Kern H (1986) Naturally occurring fluorescent pseudomonads involved in suppression of black root rot of tobacco. Phytopathology 76:181–185CrossRefGoogle Scholar
  266. Stutz E, Kahr G, Défago G (1989) Clays involved in suppression of tobacco black root rot by a strain of Pseudomonas fluorescens. Soil Biol Biochem 21:361–366CrossRefGoogle Scholar
  267. Suzuki S, He Y, Oyaizu H (2003) Indole-3-acetic acid production in Pseudomonas fluorescens HP72 and its association with suppression of creeping bentgrass brown patch. Curr Microbiol 47:138–143PubMedCrossRefGoogle Scholar
  268. Szekeres A, Leitgeb B, Kredics L, Antal Z, Hatvani L, Manczinger L, Vágvölgyi C (2005) Peptaibols and related peptaibiotics of Trichoderma. Acta Microbiol Immunol Hung 52:137–168PubMedCrossRefGoogle Scholar
  269. Thompson DC, Kobayashi DY, Clarke BB (1998) Suppression of summer patch by rhizosphere competent bacteria and their establishment on Kentucky bluegrass. Soil Biol Biochem 30:257–263CrossRefGoogle Scholar
  270. 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 13:1293–1300PubMedCrossRefGoogle Scholar
  271. Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biol Biochem 31:1847–1852CrossRefGoogle Scholar
  272. Thomashow LS, Weller DM (1988) Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J Bacteriol 170:3499–3508Google Scholar
  273. Touré Y, Ongena M, Jacques P, Guiro A, Thonart P (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96:1151–1160PubMedCrossRefGoogle Scholar
  274. Trejo-Estrada SR, Paszczynski A, Crawford DL (1998) Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9. J Ind Microbiol Biotechnol 21:81–90CrossRefGoogle Scholar
  275. Troxler J, Zala M, Moënne-Loccoz Y, Keel C, Défago G (1997a) Predominance of nonculturable cells of the biocontrol strain Pseudomonas fluorescens CHA0 in the surface horizon of large outdoor lysimeters. Appl Environ Microbiol 63:3776–3782PubMedGoogle Scholar
  276. Troxler J, Zala M, Natsch A, Moënne-Loccoz Y, Défago G (1997b) Autecology of the biocontrol strain Pseudomonas fluorescens CHA0 in the rhizosphere and inside roots at later stages of plant development. FEMS Microbiol Ecol 24:287–287Google Scholar
  277. Uroz S, Chhabra SR, Camara M, Williams P, Oger P, Dessaux Y (2005) N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151:3313–3322PubMedCrossRefGoogle Scholar
  278. van Dijk K, Nelson EB (1998) Inactivation of seed exudate stimulants of Pythium ultimum sporangium germination by biocontrol strains of Enterobacter cloacae and other seed-associated bacteria. Soil Biol Biochem 30:183–192CrossRefGoogle Scholar
  279. 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 66:5340–5347PubMedCrossRefGoogle Scholar
  280. van Elsas JD, Speksnijder AJ, van Overbeek LS (2008) A procedure for the metagenomics exploration of disease-suppressive soils. J Microbiol Methods 75:515–522PubMedCrossRefGoogle Scholar
  281. van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254CrossRefGoogle Scholar
  282. Viterbo ADA, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Appl Soil Ecol 8:737–746Google Scholar
  283. Voisard C, Keel C, Haas D, Défago G (1989) Cyanide production by Pseudomonas fluorescens helps suppress back root-rot of tobacco under gnotobiotic conditions. EMBO J 8:351–358PubMedGoogle Scholar
  284. Walsh UF, Moënne-Loccoz Y, Tichy H-V, Gardner A, Corkery DM, Lorkhe S, O’Gara F (2003) Residual impact of the biocontrol inoculant Pseudomonas fluorescens F113 on the resident population of rhizobia nodulating a red clover rotation crop. Microb Ecol 45:145–155PubMedCrossRefGoogle Scholar
  285. Wang C, Knill E, Glick BR, Défago G (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can J Microbiol 46:898–907PubMedGoogle Scholar
  286. Wang CX, Ramette A, Punjasamarnwong P, Zala M, Natsch A, Moënne-Loccoz Y, Défago G (2001) Cosmopolitan distribution of phlD-containing dicotyledonous crop-associated biocontrol pseudomonads of worldwide origin. FEMS Microbiol Ecol 37:105–116CrossRefGoogle Scholar
  287. Weibelzahl-Fulton E, Dickson W, Whitty EB (1996) Suppression of Meloidogyne incognita and M. javanica by Pasteuria penetrans in field. J Nematol 28:43–49PubMedGoogle Scholar
  288. Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256PubMedCrossRefGoogle Scholar
  289. Weller DM, Raaijmakers JM, McSpadden Gardener BB (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348PubMedCrossRefGoogle Scholar
  290. Weller DM, Landa BB, Mavrodi OV, Schroeder KL, De La Fuente L, Bankhead SB, Molar RA, Bonsall RF, Mavrodi DV, Thomashow LS (2007) Role of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biol 9:4–20PubMedCrossRefGoogle Scholar
  291. Westphal A, Becker JO (1999) Biological suppression and natural population decline of Heterodera schachtii in a California field. Phytopathology 89:434–440PubMedCrossRefGoogle Scholar
  292. Westphal A, Becker JO (2000) Transfer of biological soil suppressiveness against Heterodera schachtii. Phytopathology 90:401–406PubMedCrossRefGoogle Scholar
  293. Xiao K, Kinkel LL, Samac DA (2002) Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol Control 23:285–295CrossRefGoogle Scholar
  294. Xiao-Yan S, Qing-Tao S, Shu-Tao X, Xiu-Lan C, Cai-Yun S, Yu-Zhong Z (2006) Broad-spectrum antimicrobial activity and high stability of trichokonins from Trichoderma koningii SMF2 against plant pathogens. FEMS Microbiol Lett 260:119–125PubMedCrossRefGoogle Scholar
  295. Yan ZN, Reddy MS, Ryu CM, McInroy JA, Wilson M, Kloepper JW (2002) Induced systemic protection against tomato late blight elicited by plant growth-promoting rhizobacteria. Phytopathology 92:1329–1333PubMedCrossRefGoogle Scholar
  296. Yedidia I, Benhamou N, Kapulnik Y, Chet I (2000) Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol Biochem 38:863–873CrossRefGoogle Scholar
  297. Yedidia I, Shoresh M, Kerem Z, Benhamou N, Kapulnik Y, Chet I (2003) Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl Environ Microbiol 69:7343–7353PubMedCrossRefGoogle Scholar
  298. Yin B, Valinsky L, Gao XB, Becker JO, Borneman J (2003a) Bacterial rRNA genes associated with soil suppressiveness against the plant-parasitic nematode Heterodera schachtii. Appl Environ Microbiol 69:1573–1580PubMedCrossRefGoogle Scholar
  299. Yin B, Valinsky L, Gao XB, Becker JO, Borneman J (2003b) Identification of fungal rDNA associated with soil suppressiveness against Heterodera schachtii using oligonucleotide fingerprinting. Phytopathology 93:1006–1013PubMedCrossRefGoogle Scholar
  300. Yoon J-H, Lee J-K, Jung S-Y, Kim J-A, Kim H-K, Oh T-K (2006) Nocardioides kongjuensis sp. nov., an N-acylhomoserine lactone-degrading bacterium. Int J Syst Evol Microbiol 56:1783–1787PubMedCrossRefGoogle Scholar
  301. Yoshida S, Hiradate S, Tsukamoto T, Hatakeda K, Shirata A (2001) Antimicrobial activity of culture filtrate of Bacillus amyloliquefaciens RC-2 isolated from mulberry leaves. Phytopathology 91:181–187PubMedCrossRefGoogle Scholar
  302. Yuan WM, Crawford DL (1995) Characterization of Streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and seed rots. Appl Environ Microbiol 61:3119–3128PubMedGoogle Scholar
  303. Zhang L, Birch RG (1997a) Mechanisms of biocontrol by Pantoea dispersa of sugar cane leaf scald disease caused by Xanthomonas albilineans. J Appl Microbiol 82:448–454PubMedCrossRefGoogle Scholar
  304. Zhang L, Birch RG (1997b) The gene for albicidin detoxification from Pantoea dispersa encodes an esterase and attenuates pathogenicity of Xanthomonas albilineans to sugarcane. Proc Natl Acad Sci USA 94:9984–9989PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Université de LyonLyonFrance
  2. 2.Université Lyon 1VilleurbanneFrance
  3. 3.CNRS, UMR5557, Ecologie MicrobienneVilleurbanneFrance
  4. 4.Biology Centre of the Academy of Sciences of the Czech RepublicInstitute of Soil BiologyČeské BudějoviceCzech Republic
  5. 5.UMR CNRS 5557 Ecologie Microbienne, Universitá Lyon 1Villeurbanne cedexFrance

Personalised recommendations