1887

Abstract

, a non-pathogenic soil-inhabiting oomycete, colonizes the root ecosystem of many crop species. Whereas most members in the genus are plant pathogens, distinguishes itself from the pathogenic species by its ability to protect plants from biotic stresses in addition to promoting plant growth. The success of at controlling soilborne pathogens is partly associated with direct antagonism mediated by mycoparasitism and antimicrobial compounds. Interestingly, has evolved with specific mechanisms to attack its prey even when these belong to closely related species. Of particular relevance is the question of how distinguishes between self- and non-self cell wall degradation during the mycoparasitic process of pathogenic oomycete species. The ability of to enter and colonize the root system before rapidly degenerating is one of the most striking features that differentiate it from all other known biocontrol fungal agents. In spite of this atypical behaviour, sensitizes the plant to defend itself through the production of at least two types of microbe-associated molecular patterns, including oligandrin and cell wall protein fractions, which appear to be closely involved in the early events preceding activation of the jasmonic acid- and ethylene-dependent signalling pathways and subsequent localized and systemic induced resistance. The aim of this review is to highlight the expanding knowledge of the mechanisms by which provides beneficial effects to plants and to explore the potential use of this oomycete or its metabolites as new disease management strategies.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.061457-0
2012-11-01
2020-04-05
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/11/2679.html?itemId=/content/journal/micro/10.1099/mic.0.061457-0&mimeType=html&fmt=ahah

References

  1. Ahn I. P., Lee S. W., Suh S. C.. ( 2007;). Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol Plant Microbe Interact20:759–768 [CrossRef][PubMed]
    [Google Scholar]
  2. Al-Rawahi A. K., Hancock J. G.. ( 1997;). Rhizosphere competence of Pythium oligandrum. Phytopathology87:951–959 [CrossRef][PubMed]
    [Google Scholar]
  3. Alabouvette C., Olivain C., Steinberg C.. ( 2006;). Biological control of plant diseases: the European situation. Eur J Plant Pathol114:329–341 [CrossRef]
    [Google Scholar]
  4. Alabouvette C., Olivain C., Migheli Q., Steinberg C.. ( 2009;). Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. New Phytol184:529–544 [CrossRef][PubMed]
    [Google Scholar]
  5. Ali M. S. A. M.. ( 1985;). Pythium populations in Middle Eastern soils relative to different cropping practices. Trans Br Mycol Soc84:695–700 [CrossRef]
    [Google Scholar]
  6. Benhamou N.. ( 2009;). La résistance chez les plantes: principes de la stratégie defensive et applications agronomiques Paris: Lavoisier, Tec & Doc;
    [Google Scholar]
  7. Benhamou N., Chet I.. ( 1997;). Cellular and molecular mechanisms involved in the interaction between Trichoderma harzianum and Pythium ultimum. Appl Environ Microbiol63:2095–2099[PubMed]
    [Google Scholar]
  8. Benhamou N., Kloepper J. W., Quadt-Hallman A., Tuzun S.. ( 1996;). Induction of defense-related ultrastructural modifications in pea root tissues inoculated with endophytic bacteria. Plant Physiol112:919–929[PubMed]
    [Google Scholar]
  9. Benhamou N., Rey P., Chérif M., Hockenhull J., Tirilly Y.. ( 1997;). Treatment with the mycoparasite Pythium oligandrum triggers induction of defense-related reactions in tomato roots when challenged with Fusarium oxsporum f. sp. radicis-lycopersici. Phytopathology87:108–122 [CrossRef][PubMed]
    [Google Scholar]
  10. Benhamou N., Rey P., Picard K., Tirilly Y.. ( 1999;). Ultrastructural and cytochemical aspects of the interaction between the mycoparasite, Pythium oligandrum and soilborne pathogens. Phytopathology89:506–517 [CrossRef][PubMed]
    [Google Scholar]
  11. Benhamou N., Bélanger R. R., Rey P., Tirilly Y.. ( 2001;). Oligandrin, the elicitin-like protein produced by the mycoparasite Pythium oligandrum, induces systemic resistance to Fusarium crown and root rot in tomato plants. Plant Physiol Biochem39:681–696 [CrossRef]
    [Google Scholar]
  12. Benhamou N., Garand C., Goulet A.. ( 2002;). Ability of nonpathogenic Fusarium oxysporum strain Fo47 to induce resistance against Pythium ultimum infection in cucumber. Appl Environ Microbiol68:4044–4060 [CrossRef][PubMed]
    [Google Scholar]
  13. Benítez T., Rincón A. M., Limón M. C., Codón A. C.. ( 2004;). Biocontrol mechanisms of Trichoderma strains. Int Microbiol7:249–260[PubMed]
    [Google Scholar]
  14. Berg G.. ( 2009;). Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol84:11–18 [CrossRef][PubMed]
    [Google Scholar]
  15. Blair J. E., Coffey M. D., Park S. Y., Geiser D. M., Kang S.. ( 2008;). A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genet Biol45:266–277 [CrossRef][PubMed]
    [Google Scholar]
  16. Bradshaw-Smith R. P., Whalley W. M., Craig G. D.. ( 1991;). Interactions between Pythium oligandrum and the fungal footrot pathogens of peas. Mycol Res95:861–865 [CrossRef]
    [Google Scholar]
  17. Broeckling C. D., Broz A. K., Bergelson J., Manter D. K., Vivanco J. M.. ( 2008;). Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol74:738–744 [CrossRef][PubMed]
    [Google Scholar]
  18. Brozova J.. ( 2002;). Exploitation of the mycoparasitic fungus Pythium oligandrum in plant protection. Plant Prot Sci38:29–35
    [Google Scholar]
  19. Cooney T. P., Nonhebel H. M.. ( 1991;). Biosynthesis of indole-3-acetic acid in tomato shoots: measurement, mass spectral identification and incorporation of 2H from 2H2O into indole-3-acetic acid, D- and L-tryptophan, indole-3-pyruvate and tryptamine. Planta184:368–376 [CrossRef]
    [Google Scholar]
  20. Cordier C., Alabouvette C.. ( 2009;). Effects of the introduction of a biocontrol strain of Trichoderma atroviride on non target soil micro-organisms. Eur J Soil Biol45:267–274 [CrossRef]
    [Google Scholar]
  21. Djonović S., Pozo M. J., Dangott L. J., Howell C. R., Kenerley C. M.. ( 2006;). Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microbe Interact19:838–853 [CrossRef][PubMed]
    [Google Scholar]
  22. Drechsler C.. ( 1943;). Two species of Pythium occurring in southern States. Phytopathology33:261–299
    [Google Scholar]
  23. Druzhinina I. S., Seidl-Seiboth V., Herrera-Estrella A., Horwitz B. A., Kenerley C. M., Monte E., Mukherjee P. K., Zeilinger S., Grigoriev I. V., Kubicek C. P.. ( 2011;). Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol9:749–759 [CrossRef][PubMed]
    [Google Scholar]
  24. Edel-Hermann V., Brenot S., Gautheron N., Aimé S., Alabouvette C., Steinberg C.. ( 2009;). Ecological fitness of the biocontrol agent Fusarium oxysporum Fo47 in soil and its impact on the soil microbial communities. FEMS Microbiol Ecol68:37–45 [CrossRef][PubMed]
    [Google Scholar]
  25. El-Katatny M. H., Abdelzaher H. M. A., Shoulkamy M. A.. ( 2006;). Antagonistic actions of Pythium oligandrum and Trichoderma harzianum against phytopathogenic fungi (Fusarium oxysporum and Pythium ultimum var. ultimum). Arch Phytopathology Plant Prot39:289–301 [CrossRef]
    [Google Scholar]
  26. Ezziyyani M., Requena M. E., Egea-Gilabert C., Candela M. E.. ( 2007;). Biological control of Phytophthora root rot of pepper using Trichoderma harzianum and Streptomyces rochei in combination. J Phytopathol155:342–349 [CrossRef]
    [Google Scholar]
  27. Flores A., Chet I., Herrera-Estrella A.. ( 1997;). Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1. Curr Genet31:30–37 [CrossRef][PubMed]
    [Google Scholar]
  28. Foley M., Deacon J. W.. ( 1985;). Isolation of Pythium oligandrum and other necrotrophic mycoparasites from soil. Trans Br Mycol Soc85:631–639 [CrossRef]
    [Google Scholar]
  29. Frankenberger W. T., Arshad M.. ( 1995;). Phytohormones in Soil: Microbial Production and Function Dekker M.. New York: Taylor & Francis;
    [Google Scholar]
  30. Garcia-Brugger A., Lamotte O., Vandelle E., Bourque S., Lecourieux D., Poinssot B., Wendehenne D., Pugin A.. ( 2006;). Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Interact19:711–724 [CrossRef][PubMed]
    [Google Scholar]
  31. Genin S., Denny T. P.. ( 2012;). Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol50:67–89 [CrossRef][PubMed]
    [Google Scholar]
  32. Gruber S., Seidl-Seiboth V.. ( 2012;). Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology158:26–34 [CrossRef][PubMed]
    [Google Scholar]
  33. Guetsky R., Shtienberg D., Elad Y., Dinoor A.. ( 2001;). Combining biocontrol agents to reduce the variability of biological control. Phytopathology92:976–985 [CrossRef][PubMed]
    [Google Scholar]
  34. 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. Phytopathology92:976–985 [CrossRef][PubMed]
    [Google Scholar]
  35. Harman G. E.. ( 2006;). Overview of mechanisms and uses of Trichoderma spp. Phytopathology96:190–194 [CrossRef][PubMed]
    [Google Scholar]
  36. Harman G. E., Howell C. R., Viterbo A., Chet I., Lorito M.. ( 2004;). Trichoderma species – opportunistic, avirulent plant symbionts. Nat Rev Microbiol2:43–56 [CrossRef][PubMed]
    [Google Scholar]
  37. Harman G. E., Herrera-Estrella A. H., Horwitz B. A., Lorito M.. ( 2012;). Special issue: Trichoderma: from basic biology to biotechnology. Microbiology158:1–2 [CrossRef][PubMed]
    [Google Scholar]
  38. Hase S., Shimizu A., Nakaho K., Takenaka S., Takahashi H.. ( 2006;). Induction of transient ethylene and reduction in severity of tomato bacterial wilt by Pythium oligandrum. Plant Pathol55:537–543 [CrossRef]
    [Google Scholar]
  39. Hase S., Takahashi S., Takenaka S., Nakaho K., Arie T., Seo S., Ohashi Y., Takahashi H.. ( 2008;). Involvement of jasmonic acid signalling in bacterial wilt disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathol57:870–876 [CrossRef]
    [Google Scholar]
  40. Heller J., Tudzynski P.. ( 2011;). Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol49:369–390 [CrossRef][PubMed]
    [Google Scholar]
  41. Helman Y., Burdman S., Okon Y.. ( 2011;). Plant growth promotion by rhizosphere bacteria through direct effects. Beneficial Microorganisms in Multicellular Life Forms89–103 Rosenberg B., Gophna U.. Berlin: Springer; [CrossRef]
    [Google Scholar]
  42. Hermosa R., Viterbo A., Chet I., Monte E.. ( 2012;). Plant-beneficial effects of Trichoderma and of its genes. Microbiology158:17–25 [CrossRef][PubMed]
    [Google Scholar]
  43. Horner N. R., Grenville-Briggs L. J., van West P.. ( 2012;). The oomycete Pythium oligandrum expresses putative effectors during mycoparasitism of Phytophthora infestans and is amenable to transformation. Fungal Biol116:24–41 [CrossRef][PubMed]
    [Google Scholar]
  44. Huang Z. Y., Bonsall R. F., Mavrodi D. V., Weller D. M., Thomashow L. S.. ( 2004;). Transformation of Pseudomonas fluorescens with genes for biosynthesis of phenazine-1-carboxylic acid improves biocontrol of rhizoctonia root rot and in situ antibiotic production. FEMS Microbiol Ecol49:243–251 [CrossRef][PubMed]
    [Google Scholar]
  45. Ikeda S., Shimizu A., Shimizu S., Takahashi H., Takenaka S.. ( 2012;). Biocontrol of black scurf on potato by seed tuber treatment with Pythium oligandrum.. Biol Control60:297–304 [CrossRef]
    [Google Scholar]
  46. Jones J. D., Dangl J. L.. ( 2006;). The plant immune system. Nature444:323–329 [CrossRef][PubMed]
    [Google Scholar]
  47. Karaca G., Tepedelen G., Belghouthi A., Paul B.. ( 2008;). A new mycoparasite, Pythium lycopersicum, isolated in Isparta, Turkey: morphology, molecular characteristics, and its antagonism with phytopathogenic fungi. FEMS Microbiol Lett288:163–170 [CrossRef][PubMed]
    [Google Scholar]
  48. Karpouzas D. G., Karatasas A., Spiridaki E., Rousidou C., Bekris F., Omirou M., Ehaliotis C., Papadopoulou K. K.. ( 2011;). Impact of a beneficial and of a pathogenic Fusarium strain on the fingerprinting-based structure of microbial communities in tomato (Lycopersicon esculentum Mill.) rhizosphere. Eur J Soil Biol47:400–408 [CrossRef]
    [Google Scholar]
  49. Kawamura Y., Takenaka S., Hase S., Kubota M., Ichinose Y., Kanayama Y., Nakaho K., Klessig D. F., Takahashi H.. ( 2009;). Enhanced defense responses in Arabidopsis induced by the cell wall protein fractions from Pythium oligandrum require SGT1, RAR1, NPR1 and JAR1. Plant Cell Physiol50:924–934 [CrossRef][PubMed]
    [Google Scholar]
  50. Latijnhouwers M., de Wit P. J. G. M., Govers F.. ( 2003;). Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol11:462–469 [CrossRef][PubMed]
    [Google Scholar]
  51. Le Floch G., Rey P., Déniel F., Benhamou N., Picard K., Tirilly Y.. ( 2003a;). Enhancement of development and induction of resistance in tomato plants by the antagonist, Pythium oligandrum. Agronomie23:455–460 [CrossRef]
    [Google Scholar]
  52. Le Floch G., Rey P., Benizri E., Benhamou N., Tirilly Y.. ( 2003b;). Impact of auxin-compounds produced by the antagonistic fungus Pythium oligandrum or the minor pathogen Pythium group F on plant growth. Plant Soil257:459–470 [CrossRef]
    [Google Scholar]
  53. Le Floch G., Benhamou N., Mamaca E., Salerno M. I., Tirilly Y., Rey P.. ( 2005;). Characterisation of the early events in atypical tomato root colonisation by a biocontrol agent, Pythium oligandrum. Plant Physiol Biochem43:1–11 [CrossRef][PubMed]
    [Google Scholar]
  54. Le Floch G., Tambong J., Vallance J., Tirilly Y., Lévesque A., Rey P.. ( 2007;). Rhizosphere persistence of three Pythium oligandrum strains in tomato soilless culture assessed by DNA macroarray and real-time PCR. FEMS Microbiol Ecol61:317–326 [CrossRef][PubMed]
    [Google Scholar]
  55. Le Floch G., Vallance J., Benhamou N., Rey P.. ( 2009;). Combining the oomycete Pythium oligandrum with two other antagonistic fungi: Root relationships and tomato grey mold biocontrol. Biol Control50:288–298 [CrossRef]
    [Google Scholar]
  56. Lévesque C. A.. ( 2011;). Fifty years of oomycetes: from consolidation to evolutionary and genomic exploration. Fungal Divers50:35–46 [CrossRef]
    [Google Scholar]
  57. Lévesque C. A., de Cock A. W. A. M.. ( 2004;). Molecular phylogeny and taxonomy of the genus Pythium. Mycol Res108:1363–1383 [CrossRef][PubMed]
    [Google Scholar]
  58. Lévesque C. A., Brouwer H., Cano L., Hamilton J. P., Holt C., Huitema E., Raffaele S., Robideau G. P., Thines M.. & other authors ( 2010;). Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol11:R73 [CrossRef][PubMed]
    [Google Scholar]
  59. Lherminier J., Benhamou N., Larrue J., Milat M. L., Boudon-Padieu E., Nicole M., Blein J. P.. ( 2003;). Cytological characterization of elicitin-induced protection in tobacco plants infected by Phytophthora parasitica or Phytoplasma. Phytopathology93:1308–1319 [CrossRef][PubMed]
    [Google Scholar]
  60. Lifshitz R., Stanghellini M. E., Baker R.. ( 1984;). A new species of Pythium isolated from soil in Colorado. Mycotaxon20:373–379
    [Google Scholar]
  61. Lodha B. C., Webster J. W.. ( 1990;). Pythium acanthophoron, a mycoparasite rediscovered in India and Britain. Mycol Res94:1006–1008 [CrossRef]
    [Google Scholar]
  62. Lorito M., Woo S. L., Harman G. E., Monte E.. ( 2010;). Translational research on Trichoderma: from ’omics to the field. Annu Rev Phytopathol48:395–417 [CrossRef][PubMed]
    [Google Scholar]
  63. Martinez C., Blanc F., Le Claire E., Besnard O., Nicole M., Baccou J. C.. ( 2001;). Salicylic acid and ethylene pathways are differentially activated in melon cotyledons by active or heat-denatured cellulase from Trichoderma longibrachiatum. Plant Physiol127:334–344 [CrossRef][PubMed]
    [Google Scholar]
  64. Masunaka A., Nakaho K., Sakai M., Takahashi H., Takenaka S.. ( 2009;). Visualization of Ralstonia solanacearum cells during biocontrol of bacterial wilt disease in tomato with Pythium oligandrum. J Gen Plant Pathol75:281–287 [CrossRef]
    [Google Scholar]
  65. Masunaka A., Sekiguchi H., Takahashi H., Takenaka S.. ( 2010;). Distribution and expression of elicitin-like protein genes of the biocontrol agent Pythium oligandrum. J Phytopathol158:417–426 [CrossRef]
    [Google Scholar]
  66. McQuilken M. P., Whipps J. M., Cooke R. C.. ( 1990;). Control of damping-off in cress and sugar-beet by commercial seed-coating with Pythium oligandrum. Plant Pathol39:452–462 [CrossRef]
    [Google Scholar]
  67. Mohamed N., Lherminier J., Farmer M. J., Fromentin J., Béno N., Houot V., Milat M. L., Blein J. P.. ( 2007;). Defense responses in grapevine leaves against Botrytis cinerea induced by application of a Pythium oligandrum strain or its elicitin, oligandrin, to roots. Phytopathology97:611–620 [CrossRef][PubMed]
    [Google Scholar]
  68. Mukherjee P. K., Latha J., Hadar R., Horwitz B. A.. ( 2003;). TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot Cell2:446–455 [CrossRef][PubMed]
    [Google Scholar]
  69. Picard K., Tirilly Y., Benhamou N.. ( 2000a;). Cytological effects of cellulases in the parasitism of Phytophthora parasitica by Pythium oligandrum. Appl Environ Microbiol66:4305–4314 [CrossRef][PubMed]
    [Google Scholar]
  70. Picard K., Ponchet M., Blein J. P., Rey P., Tirilly Y., Benhamou N.. ( 2000b;). Oligandrin. A proteinaceous molecule produced by the mycoparasite Pythium oligandrum induces resistance to Phytophthora parasitica infection in tomato plants. Plant Physiol124:379–396 [CrossRef][PubMed]
    [Google Scholar]
  71. Plett J. M., Kemppainen M., Kale S. D., Kohler A., Legué V., Brun A., Tyler B. M., Pardo A. G., Martin F.. ( 2011;). A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol21:1197–1203 [CrossRef][PubMed]
    [Google Scholar]
  72. Ponchet M., Panabières F., Milat M.-L., Mikes V., Montillet J. L., Suty L., Triantaphylides C., Tirilly Y., Blein J. P.. ( 1999;). Are elicitins cryptograms in plant-Oomycete communications?. Cell Mol Life Sci56:1020–1047 [CrossRef][PubMed]
    [Google Scholar]
  73. Raimam M. P., Albino U., Cruz M. F., Lovato G. M., Spago F., Ferracin T. P., Lima D. S., Goulart T., Bernardi C. M.. & other authors ( 2007;). Interaction among free-living N-fixing bacteria isolated from Drosera villosa var. villosa and AM fungi (Glomus clarum) in rice (Oryza sativa). Appl Soil Ecol35:25–34 [CrossRef]
    [Google Scholar]
  74. Rey P., Benhamou N., Tirilly Y.. ( 1998a;). Ultrastructural and cytochemical investigations of asymptomatic infection by Pythium spp. Phytopathology88:234–244 [CrossRef][PubMed]
    [Google Scholar]
  75. Rey P., Benhamou N., Wulff E., Tirilly Y.. ( 1998b;). Interactions between tomato (Lycopersicon esculentum) root tissues and the mycoparasite Pythium oligandrum. Physiol Mol Plant Pathol53:105–122 [CrossRef]
    [Google Scholar]
  76. Rey P., Leucart S., Desilets H., Bélanger R. R., Larue J. P., Tirilly Y.. ( 2001;). Production of auxin and tryptophol by Pythium ultimum and minor pathogen, Pythium group F. Possible role in pathogenesis. Eur J Plant Pathol107:895–904 [CrossRef]
    [Google Scholar]
  77. Rey P., Le Floch G., Benhamou N., Salerno M. I., Thuillier E., Tirilly Y.. ( 2005;). Interactions between the mycoparasite Pythium oligandrum and two types of sclerotia of plant-pathogenic fungi. Mycol Res109:779–788 [CrossRef][PubMed]
    [Google Scholar]
  78. Rey P., Le Floch G., Benhamou N., Tirilly Y.. ( 2008;). Pythium oligandrum biocontrol: its relationships with fungi and plants. Plant-Microbe Interactions43–67 Ait-Barka E., Clément C.. India: Research Signpost;
    [Google Scholar]
  79. Ribeiro W. R. C., Butler E. E.. ( 1992;). Isolation of mycoparasitic species of Pythium with spiny oogonia from soil in California. Mycol Res96:857–862 [CrossRef]
    [Google Scholar]
  80. Rybicka H.. ( 1981;). Tryptophan in root exudate of mock orange and tomato. Acta Physiol Plant3:95–98
    [Google Scholar]
  81. Seidl V., Song L., Lindquist E., Gruber S., Koptchinskiy A., Zeilinger S., Schmoll M., Martínez P., Sun J.. & other authors ( 2009;). Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey. BMC Genomics10:567 [CrossRef][PubMed]
    [Google Scholar]
  82. Sendon P. M., Seo H. S., Song J. T.. ( 2011;). Salicylic acid signaling: biosynthesis, metabolism, and crosstalk with jasmonic acid. J Korean Soc Appl Biol Chem54:501–506
    [Google Scholar]
  83. Shoresh M., Yedidia I., Chet I.. ( 2005;). Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology95:76–84 [CrossRef][PubMed]
    [Google Scholar]
  84. Silby M. W., Levy S. B.. ( 2004;). Use of in vivo expression technology to identify genes important in growth and survival of Pseudomonas fluorescens Pf0-1 in soil: discovery of expressed sequences with novel genetic organization. J Bacteriol186:7411–7419 [CrossRef][PubMed]
    [Google Scholar]
  85. Taiz L., Zeiger E.. ( 1998;). Auxins. Plant Physiology543–589 Taiz L., Zeiger E.. Sunderland, MA, USA: Sinauer Associates;
    [Google Scholar]
  86. Takahashi H., Ishihara T., Hase S., Chiba A., Nakaho K., Arie T., Teraoka T., Iwata M., Tugane T.. & other authors ( 2006;). Beta-cyanoalanine synthase as a molecular marker for induced resistance by fungal glycoprotein elicitor and commercial plant activators. Phytopathology96:908–916 [CrossRef][PubMed]
    [Google Scholar]
  87. Takemoto D., Tanaka A., Scott B.. ( 2007;). NADPH oxidases in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol44:1065–1076 [CrossRef][PubMed]
    [Google Scholar]
  88. Takenaka S., Tamagake H.. ( 2009;). Foliar spray of a cell wall protein fraction from the biocontrol agent Pythium oligandrum induces defence-related genes and increases resistance against Cercospora leaf spot in sugar beet. J Gen Plant Pathol75:340–348 [CrossRef]
    [Google Scholar]
  89. Takenaka S., Nishio Z., Nakamura Y.. ( 2003;). Induction of defense reactions in sugar beet and wheat by treatment with cell wall protein fractions from the mycoparasite Pythium oligandrum. Phytopathology93:1228–1232 [CrossRef][PubMed]
    [Google Scholar]
  90. Takenaka S., Nakamura Y., Kono T., Sekiguchi H., Masunaka A., Takahashi H.. ( 2006;). Novel elicitin-like proteins isolated from the cell wall of the biocontrol agent Pythium oligandrum induce defence-related genes in sugar beet. Mol Plant Pathol7:325–339 [CrossRef][PubMed]
    [Google Scholar]
  91. Takenaka S., Sekiguchi H., Nakaho K., Tojo M., Masunaka A., Takahashi H.. ( 2008;). Colonization of Pythium oligandrum in the tomato rhizosphere for biological control of bacterial wilt disease analyzed by real-time PCR and confocal laser-scanning microscopy. Phytopathology98:187–195 [CrossRef][PubMed]
    [Google Scholar]
  92. Takenaka S., Yamaguchi K., Masunaka A., Hase S., Inoue T., Takahashi H.. ( 2011;). Implications of oligomeric forms of POD-1 and POD-2 proteins isolated from cell walls of the biocontrol agent Pythium oligandrum in relation to their ability to induce defense reactions in tomato. J Plant Physiol168:1972–1979 [CrossRef][PubMed]
    [Google Scholar]
  93. Thines M., Kamoun S.. ( 2010;). Oomycete-plant coevolution: recent advances and future prospects. Curr Opin Plant Biol13:427–433 [CrossRef][PubMed]
    [Google Scholar]
  94. Trillas M. I., Segarra G.. ( 2009;). Interactions between non-pathogenic fungi and plants. Adv Bot Res51:321–359 [CrossRef]
    [Google Scholar]
  95. Validov S. Z., Kamilova F. D., Lugtenberg B. J. J.. ( 2011;). Monitoring of pathogenic and non-pathogenic Fusarium oxysporum strains during tomato plant infection. Microb Biotechnol4:82–88 [CrossRef][PubMed]
    [Google Scholar]
  96. Vallance J., Le Floch G., Déniel F., Barbier G., Lévesque C. A., Rey P.. ( 2009;). Influence of Pythium oligandrum biocontrol on fungal and oomycete population dynamics in the rhizosphere. Appl Environ Microbiol75:4790–4800 [CrossRef][PubMed]
    [Google Scholar]
  97. Vallance J., Déniel F., Le Floch G., Guérin-Dubrana L., Blancard D., Rey P.. ( 2011;). Pathogenic and beneficial microorganisms in soilless cultures. Agron Sustain Dev31:191–203 [CrossRef]
    [Google Scholar]
  98. Vallance J., Déniel F., Barbier G., Guérin-Dubrana L., Benhamou N., Rey P.. ( 2012;). Influence of Pythium oligandrum on the bacterial communities that colonize the nutrient solutions and the rhizosphere of tomato plants. Can J Microbiol58:1124–1134 [CrossRef][PubMed]
    [Google Scholar]
  99. Van der Ent S., Van Wees S. C. M., Pieterse C. M. J.. ( 2009;). Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry70:1581–1588 [CrossRef][PubMed]
    [Google Scholar]
  100. Van der Plaats-Niterink A. J.. ( 1981;). Monograph of the genus Pythium. Studies in Mycology, No 21. Centraalbureau voor Schimmelculcures 242 Netherlands: Baarn;
    [Google Scholar]
  101. van West P., Appiah A. A., Gow N. A. R.. ( 2003;). Advances in research on oomycete root pathogens. Physiol Mol Plant Pathol62:99–113 [CrossRef]
    [Google Scholar]
  102. Veloso J., Diaz J.. ( 2012;). Fusarium oxysporum Fo47 confers protection to pepper plants against Verticillium dahliae and Phytophthora capsici, and induces the expression of defence genes. Plant Pathol61:281–288 [CrossRef]
    [Google Scholar]
  103. Vinale F., Sivasithamparam K., Ghisalberti E. L., Marra R., Woo S. L., Lorito M.. ( 2008;). Trichoderma-plant-pathogen interactions. Soil Biol Biochem40:1–10 [CrossRef]
    [Google Scholar]
  104. Vlot A. C., Dempsey D. A., Klessig D. F.. ( 2009;). Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol47:177–206 [CrossRef][PubMed]
    [Google Scholar]
  105. Whipps J. M.. ( 2004;). Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot82:1198–1227 [CrossRef]
    [Google Scholar]
  106. Woo S. L., Lorito M.. ( 2007;). Exploiting the interactions between fungal antagonists, pathogens, and the plant for biocontrol. Novel Biotechnologies for Biocontrol Agent Enhancement and Management107–130 Vurro M., Gressel J.. Dordrecht, The Netherlands: Springer; [CrossRef]
    [Google Scholar]
  107. Woo S. L., Scala F., Ruocco M., Lorito M.. ( 2006;). The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology96:181–185 [CrossRef][PubMed]
    [Google Scholar]
  108. Yedidia I., Benhamou N., Chet I.. ( 1999;). Induction of defense responses in cucumber plants (Cucumis sativus L. ) By the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol65:1061–1070[PubMed]
    [Google Scholar]
  109. 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 Biochem38:863–873 [CrossRef]
    [Google Scholar]
  110. Yedidia I., Srivastva A. K., Kapulnik Y., Chet I.. ( 2001;). Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil235:235–242 [CrossRef]
    [Google Scholar]
  111. 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 Microbiol69:7343–7353 [CrossRef][PubMed]
    [Google Scholar]
  112. Zamioudis C., Pieterse C. M. J.. ( 2012;). Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact25:139–150 [CrossRef][PubMed]
    [Google Scholar]
  113. Zeilinger S., Galhaup C., Payer K., Woo S. L., Mach R. L., Fekete C., Lorito M., Kubicek C. P.. ( 1999;). Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet Biol26:131–140 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.061457-0
Loading
/content/journal/micro/10.1099/mic.0.061457-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error