1887

Abstract

(teleomorph ) is a fungal genus found in many ecosystems. spp. can reduce the severity of plant diseases by inhibiting plant pathogens in the soil through their highly potent antagonistic and mycoparasitic activity. Moreover, as revealed by research in recent decades, some strains can interact directly with roots, increasing plant growth potential, resistance to disease and tolerance to abiotic stresses. This mini-review summarizes the main findings concerning the –plant interaction, the molecular dialogue between the two organisms, and the dramatic changes induced by the beneficial fungus in the plant. Efforts to enhance plant resistance and tolerance to a broad range of stresses by expressing genes in the plant genome are also addressed.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.052274-0
2012-01-01
2020-08-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/1/17.html?itemId=/content/journal/micro/10.1099/mic.0.052274-0&mimeType=html&fmt=ahah

References

  1. Altomare C., Norvell W. A., Björkman T., Harman G. E.. ( 1999;). Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum rifai 1295-22. Appl Environ Microbiol65:2926–2933[PubMed]
    [Google Scholar]
  2. Bae H., Sicher R. C., Kim M. S., Kim S. H., Strem M. D., Melnick R. L., Bailey B. A.. ( 2009;). The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. . J Exp Bot60:3279–3295 [CrossRef][PubMed]
    [Google Scholar]
  3. Baker R., Elad Y., Chet I.. ( 1984;). The controlled experiment in the scientific method with special emphasis on biological control. Phytopathology74:1019–1021 [CrossRef]
    [Google Scholar]
  4. Baranski R., Klocke E., Nothnagel T.. ( 2008;). Chitinase CHIT36 from Trichoderma harzianum enhances resistance of transgenic carrot to fungal pathogens. J Phytopathol156:513–521 [CrossRef]
    [Google Scholar]
  5. Bolar J. P., Norelli J. L., Wong K. W., Hayes C. K., Harman G. E., Aldwinckle H. S.. ( 2000;). Expression of endochitinase from Trichoderma harzianum in transgenic apple increases resistance to apple scab and reduces vigor. Phytopathology90:72–77 [CrossRef][PubMed]
    [Google Scholar]
  6. Bolar J. P., Norelli J., Harman G. E., Brown S. K., Aldwinckle H. S.. ( 2001;). Synergistic activity of endochitinase and exochitinase from Trichoderma harzianum against the pathogenic fungus Venturia inaequalis in transgenic plants. Transgenic Res10:533–543 [CrossRef][PubMed]
    [Google Scholar]
  7. Brants A., Earle E. D.. ( 2001;). Transgenic tobacco cell cultures expressing a Trichoderma harzianum endochitinase gene release the enzyme into the medium. Plant Cell Rep20:73–78 [CrossRef]
    [Google Scholar]
  8. Brotman Y., Briff E., Viterbo A., Chet I.. ( 2008;). Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol147:779–789 [CrossRef][PubMed]
    [Google Scholar]
  9. Cazalé A. C., Clément M., Chiarenza S., Roncato M. A., Pochon N., Creff A., Marin E., Leonhardt N., Noël L. D.. ( 2009;). Altered expression of cytosolic/nuclear HSC70-1 molecular chaperone affects development and abiotic stress tolerance in Arabidopsis thaliana. . J Exp Bot60:2653–2664 [CrossRef][PubMed]
    [Google Scholar]
  10. Chacón M. R., Rodríguez-Galán O., Benítez T., Sousa S., Rey M., Llobell A., Delgado-Jarana J.. ( 2007;). Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. . Int Microbiol10:19–27[PubMed]
    [Google Scholar]
  11. Chang Y. C., Baker R., Kleifeld O., Chet I.. ( 1986;). Increased growth of plants in the presence of the biological control agent Trichoderma harzianum. . Plant Dis70:145–148 [CrossRef]
    [Google Scholar]
  12. Chen L. L., Yang X., Raza W., Li J., Liu Y., Qiu M., Zhang F., Shen Q.. ( 2011;). Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers. Appl Microbiol Biotechnol89:1653–1663 [CrossRef][PubMed]
    [Google Scholar]
  13. Contreras-Cornejo H. A., Macías-Rodríguez L., Cortés-Penagos C., López-Bucio J.. ( 2009;). Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. . Plant Physiol149:1579–1592 [CrossRef][PubMed]
    [Google Scholar]
  14. Dana M. M., Pintor-Toro J. A., Cubero B.. ( 2006;). Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol142:722–730 [CrossRef][PubMed]
    [Google Scholar]
  15. de Jonge R., van Esse H. P., Kombrink A., Shinya T., Desaki Y., Bours R., van der Krol S., Shibuya N., Joosten M. H. A. J., Thomma B. P. H. J.. ( 2010;). Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science329:953–955 [CrossRef][PubMed]
    [Google Scholar]
  16. De Meyer G., Bigirimana J., Elad Y., Höfte M.. ( 1998;). Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. . Eur J Plant Pathol104:279–286 [CrossRef]
    [Google Scholar]
  17. Distefano G., La Malfa S., Vitale A., Lorito M., Deng Z., Gentile A.. ( 2008;). Defence-related gene expression in transgenic lemon plants producing an antimicrobial Trichoderma harzianum endochitinase during fungal infection. Transgenic Res17:873–879 [CrossRef][PubMed]
    [Google Scholar]
  18. Dixit P., Mukherjee P. K., Sherkhane P. D., Kale S. P., Eapen S.. ( 2011;). Enhanced tolerance and remediation of anthracene by transgenic tobacco plants expressing a fungal glutathione transferase gene. J Hazard Mater192:270–276[PubMed]
    [Google Scholar]
  19. 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]
  20. Djonovic S., Vargas W. A., Kolomiets M. V., Horndeski M., Wiest A., Kenerley C. M.. ( 2007;). A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol145:875–889 [CrossRef][PubMed]
    [Google Scholar]
  21. Donoso E. P., Bustamante R. O., Carú M., Niemeyer H. M.. ( 2008;). Water deficit as a driver of the mutualistic relationship between the fungus Trichoderma harzianum and two wheat genotypes. Appl Environ Microbiol74:1412–1417 [CrossRef][PubMed]
    [Google Scholar]
  22. 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]
  23. Emani C., García J. M., Lopata-Finch E., Pozo M. J., Uribe P., Kim D. J., Sunilkumar G., Cook D. R., Kenerley C. M., Rathore K. S.. ( 2003;). Enhanced fungal resistance in transgenic cotton expressing an endochitinase gene from Trichoderma virens. . Plant Biotechnol J1:321–336 [CrossRef][PubMed]
    [Google Scholar]
  24. Engelberth J., Koch T., Schüler G., Bachmann N., Rechtenbach J., Boland W.. ( 2001;). Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol125:369–377 [CrossRef][PubMed]
    [Google Scholar]
  25. Faize M., Malnoy M., Dupuis F., Chevalier M., Parisi L., Chevreau E.. ( 2003;). Chitinases of Trichoderma atroviride induce scab resistance and some metabolic changes in two cultivars of apple. Phytopathology93:1496–1504 [CrossRef][PubMed]
    [Google Scholar]
  26. Gallou A., Cranenbrouck S., Declerck S.. ( 2009;). Trichoderma harzianum elicits defence response genes in roots of potato plantlets challenged by Rhizoctonia solani. . Eur J Plant Pathol124:219–230 [CrossRef]
    [Google Scholar]
  27. Gentile A., Deng Z., La Malfa S., Distefano G., Domina F., Vitale A., Polizzi G., Lorito M., Tribulato E.. ( 2007;). Enhanced resistance to Phoma tracheiphila and Botrytis cinerea in transgenic lemon plants expressing a Trichoderma harzianum chitinase gene. Plant Breed126:146–151 [CrossRef]
    [Google Scholar]
  28. Gravel V., Antoun V., Tweddell R. J.. ( 2007;). Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indoleacetic acid (IAA). Soil Biol Biochem39:1968–1977 [CrossRef]
    [Google Scholar]
  29. Harman G. E.. ( 2000;). Myths and dogmas of biocontrol – changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis84:377–393 [CrossRef]
    [Google Scholar]
  30. 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]
  31. Hermosa R., Botella L., Keck E., Jiménez J. A., Montero-Barrientos M., Arbona V., Gómez-Cadenas A., Monte E., Nicolás C.. ( 2011;). The overexpression in Arabidopsis thaliana of a Trichoderma harzianum gene that modulates glucosidase activity, and enhances tolerance to salt and osmotic stresses. J Plant Physiol168:1295–1302 [CrossRef][PubMed]
    [Google Scholar]
  32. Korolev N., Rav David D., Elad Y.. ( 2008;). The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. . BioControl53:667–683 [CrossRef]
    [Google Scholar]
  33. Kubicek C. P., Herrera-Estrella A., Seidl-Seiboth V., Martinez D. A., Druzhinina I. S., Thon M., Zeilinger S., Casas-Flores S., Horwitz B. A.. & other authors ( 2011;). Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma . Genome Biol12:R40 [CrossRef][PubMed]
    [Google Scholar]
  34. Kumar V., Parkhi V., Kenerley C. M., Rathore K. S.. ( 2009;). Defense-related gene expression and enzyme activities in transgenic cotton plants expressing an endochitinase gene from Trichoderma virens in response to interaction with Rhizoctonia solani. . Planta230:277–291 [CrossRef][PubMed]
    [Google Scholar]
  35. Liu M., Sun Z. X., Zhu J., Xu T., Harman G. E., Lorito M.. ( 2004;). Enhancing rice resistance to fungal pathogens by transformation with cell wall degrading enzyme genes from Trichoderma atroviride. . J Zhejiang Univ Sci5:133–136 [CrossRef][PubMed]
    [Google Scholar]
  36. Lorito M., Woo S. L., García I., Colucci G., Harman G. E., Pintor-Toro J. A., Filippone E., Muccifora S., Lawrence C. B.. & other authors ( 1998;). Genes from mycoparasitic fungi as a source for improving plant resistance to fungal pathogens. Proc Natl Acad Sci U S A95:7860–7865 [CrossRef][PubMed]
    [Google Scholar]
  37. 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]
  38. Luo Y., Zhang D. D., Dong X. W., Zhao P. B., Chen L. L., Song X. Y., Wang X. J., Chen X. L., Shi M., Zhang Y. Z.. ( 2010;). Antimicrobial peptaibols induce defense responses and systemic resistance in tobacco against tobacco mosaic virus. FEMS Microbiol Lett313:120–126 [CrossRef][PubMed]
    [Google Scholar]
  39. Martínez 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]
  40. Mastouri F., Björkman T., Harman G. E.. ( 2010;). Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology100:1213–1221 [CrossRef][PubMed]
    [Google Scholar]
  41. Masunaka A., Hyakumachi M., Takenaka S.. ( 2011;). Plant growth-promoting fungus, Trichoderma koningi suppresses isoflavonoid phytoalexin vestitol production for colonization on/in the roots of Lotus japonicus. . Microbes Environ26:128–134 [CrossRef][PubMed]
    [Google Scholar]
  42. Montero-Barrientos M., Hermosa R., Cardoza R. E., Gutiérrez S., Nicolás C., Monte E.. ( 2010;). Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J Plant Physiol167:659–665 [CrossRef][PubMed]
    [Google Scholar]
  43. Mora A., Earle E. D.. ( 2001;). Resistance to Alternaria brassicicola in transgenic broccoli expressing a Trichoderma harzianum endochitinase gene. Mol Breed8:1–9 [CrossRef]
    [Google Scholar]
  44. Morán-Diez E., Hermosa R., Ambrosino P., Cardoza R. E., Gutiérrez S., Lorito M., Monte E.. ( 2009;). The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction. Mol Plant Microbe Interact22:1021–1031 [CrossRef][PubMed]
    [Google Scholar]
  45. Pieterse C. M. J., Leon-Reyes A., Van der Ent S., Van Wees S. C. M.. ( 2009;). Networking by small-molecule hormones in plant immunity. Nat Chem Biol5:308–316 [CrossRef][PubMed]
    [Google Scholar]
  46. Rotblat B., Enshell-Seijffers D., Gershoni J. M., Schuster S., Avni A.. ( 2002;). Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J32:1049–1055 [CrossRef][PubMed]
    [Google Scholar]
  47. Ruocco M., Lanzuise S., Vinale F., Marra R., Turrà D., Woo S. L., Lorito M.. ( 2009;). Identification of a new biocontrol gene in Trichoderma atroviride: the role of an ABC transporter membrane pump in the interaction with different plant-pathogenic fungi. Mol Plant Microbe Interact22:291–301 [CrossRef][PubMed]
    [Google Scholar]
  48. Salas-Marina M. A., Silva-Flores M. A., Uresti-Rivera E. E., Castro-Longoria E., Herrera-Estrella A., Casas-Flores S.. ( 2011;). Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur J Plant Pathol131:15–26 [CrossRef]
    [Google Scholar]
  49. Segarra G., Casanova E., Bellido D., Odena M. A., Oliveira E., Trillas I.. ( 2007;). Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics7:3943–3952 [CrossRef][PubMed]
    [Google Scholar]
  50. Segarra G., Van der Ent S., Trillas I., Pieterse C. M. J.. ( 2009;). MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol (Stuttg)11:90–96 [CrossRef][PubMed]
    [Google Scholar]
  51. Seidl V., Marchetti M., Schandl R., Allmaier G., Kubicek C. P.. ( 2006;). Epl1, the major secreted protein of Hypocrea atroviridis on glucose, is a member of a strongly conserved protein family comprising plant defense response elicitors. FEBS J273:4346–4359 [CrossRef][PubMed]
    [Google Scholar]
  52. Shah J. M., Raghupathy V., Veluthambi K.. ( 2009;). Enhanced sheath blight resistance in transgenic rice expressing an endochitinase gene from Trichoderma virens. . Biotechnol Lett31:239–244 [CrossRef][PubMed]
    [Google Scholar]
  53. 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]
  54. Shoresh M., Harman G. E., Mastouri F.. ( 2010;). Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol48:21–43 [CrossRef][PubMed]
    [Google Scholar]
  55. Stepanova A. N., Yun J., Likhacheva A. V., Alonso J. M.. ( 2007;). Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell19:2169–2185 [CrossRef][PubMed]
    [Google Scholar]
  56. Stergiopoulos I., de Wit P. J.. ( 2009;). Fungal effector proteins. Annu Rev Phytopathol47:233–263 [CrossRef][PubMed]
    [Google Scholar]
  57. Tucci M., Ruocco M., De Masi L., De Palma M., Lorito M.. ( 2011;). The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol12:341–354 [CrossRef][PubMed]
    [Google Scholar]
  58. Vadassery J., Tripathi S., Prasad R., Varma A., Oelmüller R.. ( 2009;). Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. . J Plant Physiol166:1263–1274 [CrossRef][PubMed]
    [Google Scholar]
  59. Van Wees S. C. M., van der Ent S., Pieterse C. M. J.. ( 2008;). Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol11:443–448 [CrossRef]
    [Google Scholar]
  60. Vargas W. A., Djonović S., Sukno S. A., Kenerley C. M.. ( 2008;). J Biol Chem283:19804–19815[CrossRef]
    [Google Scholar]
  61. Vargas W. A., Mandawe J. C., Kenerley C. M.. ( 2009;). Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol151:792–808 [CrossRef][PubMed]
    [Google Scholar]
  62. Vinale F., Sivasithamparam K., Ghisalberti E. L., Marra R., Barbetti M. J., Li H., Woo S. L., Lorito M.. ( 2008;). A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol72:80–86 [CrossRef]
    [Google Scholar]
  63. Viterbo A., Chet I.. ( 2006;). TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol7:249–258 [CrossRef][PubMed]
    [Google Scholar]
  64. Viterbo A., Horwitz B. A.. ( 2010;). Mycoparasitism. Cellular and Molecular Biology of Filamentous Fungi676–693 Borkovich K. A., Ebbole D. J.. Washington: American Society for Microbiology;
    [Google Scholar]
  65. Viterbo A., Wiest A., Brotman Y., Chet I., Kenerley C.. ( 2007;). The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol8:737–746 [CrossRef][PubMed]
    [Google Scholar]
  66. Viterbo A., Landau U., Kim S., Chernin L., Chet I.. ( 2010;). Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett305:42–48 [CrossRef][PubMed]
    [Google Scholar]
  67. Vizcaíno J. A., Cardoza R. E., Hauser M., Hermosa R., Rey M., Llobell A., Becker J. M., Gutiérrez S., Monte E.. ( 2006;). ThPTR2, a di/tri-peptide transporter gene from Trichoderma harzianum. . Fungal Genet Biol43:234–246 [CrossRef][PubMed]
    [Google Scholar]
  68. 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]
  69. 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]
  70. Yoshioka Y., Ichikawa H., Naznin H. A., Kogure A., Hyakumachi M.. ( 2011;). Systemic resistance induced in Arabidopsis thaliana by Trichoderma asperellum SKT-1, a microbial pesticide of seedborne diseases of rice. Pest Manag Scihttp://dx.doi.org/10.1002/ps.2220 (Epub ahead of print) [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.052274-0
Loading
/content/journal/micro/10.1099/mic.0.052274-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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