1887

Abstract

spp. are widely used as biopesticides and biofertilizers to control diseases and to promote positive physiological responses in plants. and assays with CECT 2413 (T34), Gv29-8 (T87) and IMI 224801 (T7) revealed that these strains affected the growth and development of lateral roots in tomato plants in different ways. The early expression profiles of these strains were studied after 20 h of incubation in the presence of tomato plants, using a high-density oligonucleotide (HDO) microarray, and compared to the profiles in the absence of plants. Out of the total 34 138 probe sets deposited on the microarray, 1077 (3.15 %) showed a significant change of at least 2-fold in expression in the presence of tomato plants. The numbers of probe sets identified in the individual strains were 593 in T34, 336 in T87 and 94 in T7. Carbohydrate metabolism – the chitin degradation enzymes -acetylglucosamine-6-phosphate deacetylase, glucosamine-6-phosphate deaminase and chitinase – was the most significantly overrepresented process commonly observed in the three strains in early interactions with tomato plants. Strains T7 and T34, which had similar positive effects on plant development in biological assays, showed a significantly overrepresented hexokinase activity in interaction with tomato. In addition, genes encoding a 40S ribosomal protein and a P23 tumour protein were altered in both these strains.

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2012-01-01
2024-04-19
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References

  1. Alfano G., Ivey M. L. L., Cakir C., Bos J. I. B., Miller S. A., Madden L. V., Kamoun S., Hoitink H. A. J. ( 2007). Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97:429–437 [View Article][PubMed]
    [Google Scholar]
  2. Ashburner M., Ball C. A., Blake J. A., Botstein D., Butler H., Cherry J. M., Davis A. P., Dolinski K., Dwight S. S. & other authors ( 2000). Gene ontology: tool for the unification of biology. Nat Genet 25:25–29 [View Article][PubMed]
    [Google Scholar]
  3. Askolin S., Penttilä M., Wösten H. A., Nakari-Setälä T. ( 2005). The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diverse functions in fungal development. FEMS Microbiol Lett 253:281–288 [View Article][PubMed]
    [Google Scholar]
  4. Bailey B. A., Bae H., Strem M. D., Roberts D. P., Thomas S. E., Crozier J., Samuels G. J., Choi I. Y., Holmes K. A. ( 2006). Fungal and plant gene expression during the colonization of cacao seedlings by endophytic isolates of four Trichoderma species. Planta 224:1449–1464 [View Article][PubMed]
    [Google Scholar]
  5. Benítez T., Rincón A. M., Limón M. C., Codón A. C. ( 2004). Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260[PubMed]
    [Google Scholar]
  6. Brotman Y., Briff E., Viterbo A., Chet I. ( 2008). Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789 [View Article][PubMed]
    [Google Scholar]
  7. Brunner K., Peterbauer C. K., Mach R. L., Lorito M., Zeilinger S., Kubicek C. P. ( 2003). The Nag1 N-acetylglucosaminidase of Trichoderma atroviride is essential for chitinase induction by chitin and of major relevance to biocontrol. Curr Genet 43:289–295[PubMed] [CrossRef]
    [Google Scholar]
  8. Carpenter M. A., Stewart A., Ridgway H. J. ( 2005). Identification of novel Trichoderma hamatum genes expressed during mycoparasitism using subtractive hybridisation. FEMS Microbiol Lett 251:105–112 [View Article][PubMed]
    [Google Scholar]
  9. 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 Microbiol 10:19–27[PubMed]
    [Google Scholar]
  10. 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 Physiol 149:1579–1592 [View Article][PubMed]
    [Google Scholar]
  11. 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 Physiol 145:875–889 [View Article][PubMed]
    [Google Scholar]
  12. Elad Y. ( 2000). Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Prot 19:709–714 [View Article]
    [Google Scholar]
  13. Felts S. J., Toft D. O. ( 2003). p23, a simple protein with complex activities. Cell Stress Chaperones 8:108–113 [View Article][PubMed]
    [Google Scholar]
  14. Gruber S., Vaaje-Kolstad G., Matarese F., López-Mondéjar R., Kubicek C. P., Seidl-Seiboth V. ( 2011). Analysis of subgroup C of fungal chitinases containing chitin-binding and LysM modules in the mycoparasite Trichoderma atroviride . Glycobiology 21:122–133 [View Article][PubMed]
    [Google Scholar]
  15. Hermosa R., Viterbo A., Chet I., Monte E. ( 2012). Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25[PubMed] [CrossRef]
    [Google Scholar]
  16. Hölker U., Dohse J., Höfer M. ( 2002). Extracellular laccases in ascomycetes Trichoderma atroviride and Trichoderma harzianum . Folia Microbiol (Praha) 47:423–427 [View Article][PubMed]
    [Google Scholar]
  17. Howell C. R. ( 2003). Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10 [View Article]
    [Google Scholar]
  18. Howell C. R. ( 2006). Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology 96:178–180 [View Article][PubMed]
    [Google Scholar]
  19. Irizarry R. A., Hobbs B., Collin F., Beazer-Barclay Y. D., Antonellis K. J., Scherf U., Speed T. P. ( 2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264 [View Article][PubMed]
    [Google Scholar]
  20. Kiiskinen L. L., Kruus K., Bailey M., Ylösmäki E., Siika-Aho M., Saloheimo M. ( 2004). Expression of Melanocarpus albomyces laccase in Trichoderma reesei and characterization of the purified enzyme. Microbiology 150:3065–3074 [View Article][PubMed]
    [Google Scholar]
  21. 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 Biol 12:R40 [View Article][PubMed]
    [Google Scholar]
  22. Lee W. L., Bezanilla M., Pollard T. D. ( 2000). Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J Cell Biol 151:789–800 [View Article][PubMed]
    [Google Scholar]
  23. Liu P. G., Yang Q. ( 2005). Identification of genes with a biocontrol function in Trichoderma harzianum mycelium using the expressed sequence tag approach. Res Microbiol 156:416–423 [View Article][PubMed]
    [Google Scholar]
  24. Livak K. J., Schmittgen T. D. ( 2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ C t method. Methods 25:402–408 [View Article][PubMed]
    [Google Scholar]
  25. Lorito M., Woo S. L., Harman G. E., Monte E. ( 2010). Translational research on Trichoderma: from ’omics to the field. Annu Rev Phytopathol 48:395–417 [View Article][PubMed]
    [Google Scholar]
  26. Marra R., Ambrosino P., Carbone V., Vinale F., Woo S. L., Ruocco M., Ciliento R., Lanzuise S., Ferraioli S. & other authors ( 2006). Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Curr Genet 50:307–321 [View Article][PubMed]
    [Google Scholar]
  27. Martinez D., Berka R. M., Henrissat B., Saloheimo M., Arvas M., Baker S. E., Chapman J., Chertkov O., Coutinho P. M. & other authors ( 2008). Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26:553–560 [View Article][PubMed]
    [Google Scholar]
  28. Mastouri F., Björkman T., Harman G. E. ( 2010). Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100:1213–1221 [View Article][PubMed]
    [Google Scholar]
  29. Mendoza-Mendoza A., Rosales-Saavedra T., Cortés C., Castellanos-Juárez V., Martínez P., Herrera-Estrella A. ( 2007). The MAP kinase TVK1 regulates conidiation, hydrophobicity and the expression of genes encoding cell wall proteins in the fungus Trichoderma virens . Microbiology 153:2137–2147 [View Article][PubMed]
    [Google Scholar]
  30. Mikus M., Hatvani L., Neuhof T., Komoń-Zelazowska M., Dieckmann R., Schwecke T., Druzhinina I. S., von Döhren H., Kubicek C. P. ( 2009). Differential regulation and posttranslational processing of the class II hydrophobin genes from the biocontrol fungus Hypocrea atroviridis . Appl Environ Microbiol 75:3222–3229 [View Article][PubMed]
    [Google Scholar]
  31. Muñoz G., Nakari-Setälä T., Agosin E., Penttilä M. ( 1997). Hydrophobin gene srh1, expressed during sporulation of the biocontrol agent Trichoderma harzianum . Curr Genet 32:225–230 [View Article][PubMed]
    [Google Scholar]
  32. Nakari-Setälä T., Aro N., Ilmén M., Muñoz G., Kalkkinen N., Penttilä M. ( 1997). Differential expression of the vegetative and spore-bound hydrophobins of Trichoderma reesei – cloning and characterization of the hfb2 gene. Eur J Biochem 248:415–423 [View Article][PubMed]
    [Google Scholar]
  33. Park D. H., Mirabella R., Bronstein P. A., Preston G. M., Haring M. A., Lim C. K., Collmer A., Schuurink R. C. ( 2010). Mutations in γ-aminobutyric acid (GABA) transaminase genes in plants or Pseudomonas syringae reduce bacterial virulence. Plant J 64:318–330 [View Article][PubMed]
    [Google Scholar]
  34. Penttilä M., Nevalainen H., Rättö M., Salminen E., Knowles J. ( 1987). A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei . Gene 61:155–164 [View Article][PubMed]
    [Google Scholar]
  35. Prell J., Boesten B., Poole P., Priefer U. B. ( 2002). The Rhizobium leguminosarum bv. viciae VF39 γ-aminobutyrate (GABA) aminotransferase gene (gabT) is induced by GABA and highly expressed in bacteroids. Microbiology 148:615–623[PubMed]
    [Google Scholar]
  36. 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 J 32:1049–1055 [View Article][PubMed]
    [Google Scholar]
  37. Samolski I., de Luis A., Vizcaíno J. A., Monte E., Suárez M. B. ( 2009). Gene expression analysis of the biocontrol fungus Trichoderma harzianum in the presence of tomato plants, chitin, or glucose using a high-density oligonucleotide microarray. BMC Microbiol 9:217 [View Article][PubMed]
    [Google Scholar]
  38. Scherm B., Schmoll M., Balmas V., Kubicek C. P., Migheli Q. ( 2009). Identification of potential marker genes for Trichoderma harzianum strains with high antagonistic potential against Rhizoctonia solani by a rapid subtraction hybridization approach. Curr Genet 55:81–91 [View Article][PubMed]
    [Google Scholar]
  39. 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. Proteomics 7:3943–3952 [View Article][PubMed]
    [Google Scholar]
  40. Seidl V., Huemer B., Seiboth B., Kubicek C. P. ( 2005). A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS J 272:5923–5939 [View Article][PubMed]
    [Google Scholar]
  41. Seidl-Seiboth V., Gruber S., Sezerman U., Schwecke T., Albayrak A., Neuhof T., von Döhren H., Baker S. E., Kubicek C. P. ( 2011). Novel hydrophobins from Trichoderma define a new hydrophobin subclass: protein properties, evolution, regulation and processing. J Mol Evol 72:339–351 [View Article][PubMed]
    [Google Scholar]
  42. Shoresh M., Harman G. E. ( 2008). The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147:2147–2163 [View Article][PubMed]
    [Google Scholar]
  43. Shoresh M., Harman G. E., Mastouri F. ( 2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43 [View Article][PubMed]
    [Google Scholar]
  44. Solomon P. S., Oliver R. P. ( 2002). Evidence that γ-aminobutyric acid is a major nitrogen source during Cladosporium fulvum infection of tomato. Planta 214:414–420 [View Article][PubMed]
    [Google Scholar]
  45. 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 Pathol 12:341–354 [View Article][PubMed]
    [Google Scholar]
  46. van Niel E. W., Palmfeldt J., Martin R., Paese M., Hahn-Hägerdal B. ( 2004). Reappraisal of the regulation of lactococcal l-lactate dehydrogenase. Appl Environ Microbiol 70:1843–1846 [View Article][PubMed]
    [Google Scholar]
  47. 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 Physiol 151:792–808 [View Article][PubMed]
    [Google Scholar]
  48. Vinale F., Marra R., Scala F., Ghisalberti E. L., Lorito M., Sivasithamparam K. ( 2006). Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148 [View Article][PubMed]
    [Google Scholar]
  49. Viterbo A., Chet I. ( 2006). TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol 7:249–258 [View Article][PubMed]
    [Google Scholar]
  50. Viterbo A., Wiest A., Brotman Y., Chet I., Kenerley C. ( 2007). The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746 [View Article][PubMed]
    [Google Scholar]
  51. Vizcaíno J. A., González F. J., Suárez M. B., Redondo J., Heinrich J., Delgado-Jarana J., Hermosa R., Gutiérrez S., Monte E. & other authors ( 2006). Generation, annotation and analysis of ESTs from Trichoderma harzianum CECT 2413. BMC Genomics 7:193 [View Article][PubMed]
    [Google Scholar]
  52. Vizcaíno J. A., Redondo J., Suárez M. B., Cardoza R. E., Hermosa R., González F. J., Rey M., Monte E. ( 2007). Generation, annotation, and analysis of ESTs from four different Trichoderma strains grown under conditions related to biocontrol. Appl Microbiol Biotechnol 75:853–862 [View Article][PubMed]
    [Google Scholar]
  53. Woo S. L., Scala F., Ruocco M., Lorito M. ( 2006). The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology 96:181–185 [View Article][PubMed]
    [Google Scholar]
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