Gate crashing arbuscular mycorrhizas: In vivo imaging shows the extensive colonization of both symbionts by Trichoderma atroviride

Environmental Microbiology Reports

Volumn 7, Issue 1, 2015, Pages 64-77

  Lace, Beatrice ^a   Genre, Andrea ^a   Woo, Sheridan ^b   Faccio, Antonella ^c   Lorito, Matteo ^b   Bonfante, Paola ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; GIGASPORA; MEDICAGO TRUNCATULA; TRICHODERMA; TRICHODERMA ATROVIRIDE;

GREEN FLUORESCENT PROTEIN;

BARREL MEDIC; CHEMISTRY; FUNGUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT; SYMBIOSIS; TRICHODERMA;

FUNGI; GREEN FLUORESCENT PROTEINS; MEDICAGO TRUNCATULA; MYCORRHIZAE; PLANT ROOTS; SYMBIOSIS; TRICHODERMA;

EID: 84923637695     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/1758-2229.12221     Document Type: Article

References (52)

1. Atanasova, L., Le Crom, S., Gruber, S., Coulpier, F., Seidl-Seiboth, V., Kubicek, C.P., and Druzhinina, I.P. (2013) Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics 14: 121.
2. Benhamou, N., and Chet, I. (1997) Cellular and molecular mechanisms involved in the interaction between Trichoderma harzianum and Pythium ultimum. Appl Environ Microbiol 63: 2095-2099.
3. Bonfante, P. (2001) At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton. In The Mycota IX. Fungal Associations. Hock, B. (ed.). Berlin: Springer, pp. 45-91.
4. Bonfante, P., and Genre, A. (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1: 48.
5. Bonfante, P., Vian, B., Perotto, S., Faccio, A., and Knox, J.P. (1990) Cellulose and pectin localization in roots of mycorrhizal Allium porrum: labelling continuity between host cell wall and interfacial material. Planta 180: 537-547.
6. Brotman, Y., Lisec, J., Méret, M., Chet, I., Willmitzer, L., and Viterbo, A. (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 22: 139-146.
7. Brotman, Y., Landau, U., Cuadros-Inostroza, Á., Takayuki, T., Fernie, A.R., Chet, I., Viterbo, A., and Willmitzer, L. (2013) Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog 9: e1003221.
8. Brunner, K., Peterbauer, C.K., Mach, R.L., Lorito, M., Zeilinger, S., and 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.
9. Carsolio, C., Benhamou, N., Haran, S., Cortés, C., Gutiérrez, A., Chet, I., and Herrera-Estrella, A. (1999) Role of the Trichoderma harzianum endochitinase gene, ech42, in mycoparasitism. Appl Environ Microbiol 65: 929-935.
10. 2+ spiking in the legume and nonlegume root epidermis. New Phytol 189: 347-355.
11. Chacon, M.R., Rodríguez-Galán, O., Benítez, T., Sousa, S., Rey, M., Llobell, A., and Delgado-Jarana, J. (2007) Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. Int Microbiol 10: 19-27.
12. Chandanie, W.A., Kubota, M., and Hyakumachi, M. (2009) Interactions between the arbuscular mycorrhizal fungus Glomus mosseae and plant growth-promoting fungi and their significance for enhancing plant growth and suppressing damping-off of cucumber (Cucumis sativus L.). App Soil Ecol 41: 336-341.
13. De Jaeger, N., Declerck, S., and De la Providencia, I.E. (2010) Mycoparasitism of arbuscular mycorrhizal fungi: a pathway for the entry of saprotrophic fungi into roots. FEMS Microbiol Ecol 73: 312-322.
14. De Jaeger, N., de la Providencia, I.E., Rouhier, H., and Declerck, S. (2011) Co-entrapment of Trichoderma harzianum and Glomus sp. within alginate beads: impact on the arbuscular mycorrhizal fungi life cycle. J Appl Microbiol 111: 125-135.
15. Deshmukh, S., Hückelhoven, R., Schäfer, P., Imani, J., Sharma, M., Weiss, M., etal. (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. PNAS 103: 18450-18457.
16. Di Pietro, A., Lorito, M., Hayes, C.K., Broadway, R.M., and Harman, G.E. (1993) Endochitinase from Gliocladium virens: isolation, characterization and synergistic antifungal activity in combination with gliotoxin. Phytopathology 83: 308-313.
17. Djonović, S., Pozo, M.J., and Kenerley, C.M. (2006) Tvbgn3, a beta-1, 6-glucanase from the biocontrol fungus Trichoderma virens, is involved in mycoparasitism and control of Pythium ultimum. Appl Environ Microbiol 72: 7661-7670.
18. Djonović, S., Vittone, G., Mendoza-Herrera, A., and Kenerley, C.M. (2007) Enhanced biocontrol activity of Trichoderma virens transformants constitutively coexpressing beta-1, 3- and beta-1, 6-glucanase genes. Mol Plant Pathol 8: 469-480.
19. Druzhinina, I.S., Shelest, E., and Kubicek, C.P. (2012) Novel traits of Trichoderma predicted through the analysis of its secretome. FEMS Microbiol Lett 337: 1-9.
20. Genre, A., and Bonfante, P. (2007) Check-in procedures for plant cell entry by biotrophic microbes. MPMI 20: 1023-1030.
21. Genre, A., Chabaud, M., Timmers, T., Bonfante, P., and Barker, D.G. (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17: 3489-3499.
22. Genre, A., Chabaud, M., Faccio, A., Barker, D.G., and Bonfante, P. (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20: 1407-1420.
23. Genre, A., Ortu, G., Bertoldo, C., Martino, E., and Bonfante, P. (2009) Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi. Plant Physiol 149: 1424-1434.
24. Harman, G.E. (2000) Myths and dogmas of biocontrol. Changes in perceptions derived from research on Trichoderma harzianum T22. Plant Dis 84: 377-393.
25. Harman, G.E. (2011) Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytol 189: 647-649.
26. Harman, G.E., Howell, C.R., Viterbo, A., Chet, I., and Lorito, M. (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2: 43-56.
27. Howell, C.R. (2006) Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology 96: 178-180.
28. Kubicek, C.P., etal. (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12: R40.
29. Lorito, M., and Woo, S.L. (2014) Trichoderma: a multi-purpose tool for IPM. In Principles of Plant-Microbe Interactions. Lugtenberg, B. (ed.). Cham (ZG), Switzerland: Springer International Publishing, p. 9 (in press). DOI: 10.1007/978-3-319-08575-3_36.
30. Lorito, M., Harman, G.E., Hayes, C.K., Broadway, R.M., Tronsmo, A., Woo, S.L., and Di Pietro, A. (1993a) Chitinolytic enzymes produced by Trichoderma harzianum: antifungal activity of purified endochitinase and chitobiosidase. Phytopathology 83: 302-307.
31. Lorito, M., Di Pietro, A., Hayes, C.K., Woo, S., and Harman, G.E. (1993b) Antifungal, synergistic interaction between chitinolytic enzymes from Trichoderma harzianum and Enterobacter cloacae. Phytopatology 83: 721-728.
32. Lorito, M., Hayes, C.K., Di Pietro, A., Woo, S.L., and Harman, G.E. (1994) Purification, characterization and synergistic activity of a glucan 1, 3-ß-glucosidase and an N-acetyl-ß-glucosaminidase from Trichoderma harzianum. Phytopathology 84: 398-405.
33. Lorito, M., Farkas, V., Rebuffat, S., Bodo, B., and Kubicek, C.P. (1996) Cell wall synthesis is a major target of mycoparasitic antagonism by Trichoderma harzianum. J Bacteriol 178: 6382-6385.
34. Lorito, M., Woo, S.L., Harman, G.E., and Monte, E. (2010) Translational research on Trichoderma: from 'omics to the field. Annu Rev Phytopathol 48: 395-417.
35. Lu, Z., Tombolini, R., Woo, S., Lorito, M., Jansson, J.K., and Zeilinger, S. (2004) In vivo study of Trichoderma-pathogen-plant interactions using constitutive and inducible green fluorescent protein reporter. Appl Environ Microbiol 70: 3073-3081.
36. Martínez-Medina, A., Roldán, A., Albacete, A., and Pascual, J. (2011) The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry 72: 223-229.
37. Martinez, D., etal. (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26: 553-560.
38. Morán-Diez, E., Rubio, B., Domínguez, S., Hermosa, R., Monte, E., and Nicolás, C. (2012) Transcriptomic response of Arabidopsis thaliana after 24 h incubation with the biocontrol fungus Trichoderma harzianum. J Plant Physiol 169: 614-620.
39. Navazio, L., Baldan, B., Moscatiello, R., Woo, S.L., Mariani, P., and Lorito, M. (2007) Calcium-mediated perception and defense responses activated in plant cells by metabolite mixtures secreted by the biocontrol fungus Trichoderma atroviride. BMC Plant Biol 7: 41.
40. Palmieri, M.C., Perazzolli, M., Matafora, V., Moretto, M., Bachi, A., and Pertot, I. (2012) Proteomic analysis of grapevine resistance induced by Trichoderma harzianum T39 reveals specific defence pathways activated against downy mildew. J Exp Bot 63: 6237-6251.
41. Perazzolli, M., Moretto, M., Fontana, P., Ferrarini, A., Velasco, R., Moser, C., etal. (2012) Downy mildew resistance induced by Trichoderma harzianum T39 in susceptible grapevines partially mimics transcriptional changes of resistant genotypes. BMC Genomics 13: 660.
42. Rousseau, A., Benhamou, N., Chet, I., and Piché, Y. (1996) Mycoparasitism of the extramatrical phase of Glomus intraradices by Trichoderma harzianum. Phytopathology 86: 434-443.
43. Schäfer, P., Khatabi, B., and Kogel, K.H. (2007) Root cell death and systemic effects of Piriformospora indica: a study on mutualism. FEMS Microbiol Lett 275: 1-7.
44. Schirmböck, M., Lorito, M., Wang, Y.L., Hayes, C.K., Arisan-Atac, I., Scala, F., etal. (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol 60: 4364-4370.
45. Shoresh, M., Harman, G.E., and Mastouri, F. (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48: 21-43.
46. 2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151: 1197-1206.
47. Singh, S., and Parniske, M. (2012) Activation of calcium- and calmodulin-dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr Opin Plant Biol 15: 444-453.
48. Tisserant, E., etal. (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci USA 110: 20117-20122.
49. Tucci, M., Ruocco, M., De Masi, L., De Palma, M., and Lorito, M. (2011) The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol 12: 341-354.
50. Vargas, W.A., Mandawe, J.C., and 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.
51. Woo, S.L., Donzelli, B., Scala, F., Mach, R., Harman, G.E., Kubicek, C.P., etal. (1999) Disruption of the ech42 (endochitinase-encoding) gene affects biocontrol activity in Trichoderma harzianum P1. MPMI 12: 419-429.
52. Zeilinger, S., Galhaup, C., Payer, K., Woo, S.L., Mach, R.L., Fekete, C., etal. (1999) Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet Biol 26: 131-140.