Trichoderma harzianum T22 induces in maize systemic resistance against Fusarium verticillioides

Journal of Plant Pathology

Volumn 96, Issue 1, 2014, Pages 133-142

  Ferrigo, D ^a   Raiola, A ^a   Piccolo, E ^a   Scopel, C ^a   Causin, R ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Fumonisin; Fusarium verticillioides; Induced systemic resistance; Maize; Trichoderma harzianum

Indexed keywords

EID: 84897909936     PISSN: 11254653     EISSN: None     Source Type: Journal    
DOI: 10.4454/JPP.V96I1.038     Document Type: Article

References (76)

1. Agrawal G.K., Jwa N.S., Rakwal R., 2000. A novel rice (Oryza sativa L.) Acidic PR1 gene highly responsive to cut phytohormones and protein phosphatase inhibitors. Biochemical Biophysical Research Communication 274: 157-165.
2. Bacon C.W., Williamson J.W., 1992. Interactions of Fusarium moniliforme, its metabolites and bacteria with corn. Mycopathologia 117: 65-71.
3. Bacon C.W., Hinton D.M., Richardson M.D., 1994. A corn seedling assay for resistance to Fusarium moniliforme. Plant Disease 78: 302-305.
4. Bacon C.W., Hinton D.M., 1996. Symptomless endophytic colonization of maize by Fusarium moniliforme. Canadian Journal of Botany 74: 1195-1202.
5. Bacon C.W., Yates I.E., Hinton D.M., Meredith F., 2001. Biological control of Fusarium moniliforme in maize. Environmental Health Perspective 109: 325-332.
6. Bacon C.W., Glenn A.E., Yates I.E., 2008. Fusarium verticillioides: managing the endophytic association with maize for reduced fumonisins accumulation. Toxin Reviews 27: 411-446.
7. Benhamou N., Chet I., 1996. Parasitism of sclerotia of Sclerotium rolfsii by Trichoderma harzianum: ultrastructural and cytochemical aspects of the interaction. Phytopathology 86: 405-416.
8. Bennet J.V., Klich M., 2003. Mycotoxins. Clinical and Microbiological Review 16: 497-516.
9. Brotman Y., Lisec J., Méret M., Chet I., Willmitzer L., Viterbo A., 2012. Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158: 139-146.
10. Casacuberta J.M., Raventós D., Puigdoménech P., Segundo B.S., 1992. Expression of the gene encoding the PR-like protein PRms in germinating maize embryos. Molecular and General Genetics 234: 97-104.
11. Cavaglieri L., Orlando J., Rodríguez M.I., Chulze S., Etcheverry M., 2005. Biocontrol of Bacillus subtilis against Fusarium verticillioides in vitro and at the maize root level. Research Microbiology. 156: 748-754.
12. Chandra Nayaka S., Niranjana S.R., Uday Shankar A.C., Niranjan Raj S., Reddy M.S., Prakash H.S., Mortensen C.N., 2010. Seed biopriming with novel strain of Trichoderma harzianum for the control of toxigenic Fusarium verticillioides and fumonisins in maize. Archives of Phytopathology and Plant Protection 43: 264-282.
13. Chen J., Harman G.E., Comis A., Cheng G.W., 2005. Proteins related to the biocontrol of pythium damping-off in maize with Trichoderma harzianum rifai. Journal of Integrative Plant Biology 47: 988-997.
14. Cipollini D., Enright S., Traw M.B., Bergelson J., 2004. Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Molecular Ecology 13: 1643-1653.
15. 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 Physiology 145: 875-889.
16. Elad Y., 1996. Mechanisms involved in the biological control of Botrytis cinerea incited diseases. European Journal of Plant Pathology 102: 719-732.
17. Farag M.A., Fokar M., Abd H., Zhang H., Allen R.D., Paré P.W., 2005. (Z)-3-Hexenol induces defense genes and downstream metabolites in maize. Planta 220: 900-909.
18. Feussner I., Wasternack C., 2002. The lipoxygenase pathway. Annual Review of Plant Biology 53: 275-297.
19. Feys B.J., Parker J.E., 2000. Interplay of signaling pathways in plant disease resistance. Trends in Genetics 16: 449-455.
20. Folcher L., Jarry M., Weissenberger A., Gérault F., Eychenne N., Delos M., Regnault-Roger C., 2009. Comparative activity of agrochemical treatments on mycotoxin levels with regard to corn borers and Fusarium mycoflora in maize (Zea mays L.) fields. Crop Protection 28: 302-308.
21. Gallou A., Cranenbrouck S., Declerck S., 2009. Trichoderma harzianum elicits defense response genes in roots of potato plantlets challenged by Rhizoctonia solani. European Journal of Plant Pathology 124: 219-230.
22. Gao L., Smith F.A., Smith S.E., 2006. The rmc locus does not affect plant interactions or defense-related gene expression when tomato (Solanum lycopersicum) is infected with the root fungal parasite Rhizoctonia. Functional Plant Biology 33: 289-296.
23. Gao X., Brodhagen M., Isakeit T., Brown S.H., Göbel C., Betran J., Feussner I., Keller N.P., Kolomiets M.V., 2009. Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. Molecular Plant Microbe Interactions 22: 222-231.
24. Glenn A.E., Gold S.E., Bacon C.W., 2002. Fdb1 and Fdb2, Fusarium verticillioides loci necessary for detoxification of preformed antimicrobials from corn. Molecular Plant. Microbe Interactions 15: 91-101.
25. Hahlbrock K., Scheel D., 1989. Physiology and molecular biology of phenylpropanoid metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 40: 347-369.
26. Harman G.E., 2000. Myths and dogmas of biocontrol: changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Disease 84: 377-393.
27. Harman G.E., Björkman T., 1998. Potential and existing uses of Trichoderma and Gliocladium for plant disease control and plant growth enhancement. In: Trichoderma and Gliocladium Vol. 2, pp. 229-265. CRC Press, Boca Raton, FL, USA.
28. Harman G.E., Howell C.R., Viterbo A., Chet I., Lorito M., 2004a. Trichoderma species-opportunistic avirulent plant symbionts. Nature Review Microbiology 2: 43-56.
29. Harman G.E., Petzoldt R., Comis A., Chen J., 2004b. Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology 94: 147-153.
30. Howell C.R., 2002. Cotton seedling preemergence damping-off incited by Rhizopus oryzae and Pythium spp. and its biological control with Trichoderma spp. Phytopathology 92: 177-180.
31. Kato M., Hayakawa Y., Hyodo H., Ikoma Y., Yano M., 2000. Wound-induced ethylene synthesis and expression and formation of 1-Aminocyclopropane-1-Carboxylate (ACC) synthase ACC oxidase phenylalanine ammonia-lyase and peroxidase in wounded mesocarp tissue of Cucurbita maxima. Plant Cell Physiology 41: 440-447.
32. Kedera C.J., Leslie J.F., Claflin L.E., 1992. Systemic infection of corn by Fusarium moniliforme. Phytopathology 82: 1138.
33. Koike N., Hyakumachi M., Kageyama K., Tsuyumu S., Doke N., 2001. Induction of systemic resistance in cucumber against several diseases by plant growth-promoting fungi: lignification and superoxide generation. European Journal of Plant Pathology 107: 523-533.
34. Leslie J.F., 1991. Mating population in Gibberella fujikuroi (Fusarium section Liseola). Phytopathology 81: 1058-1060.
35. Logrieco A., Mulè G., Moretti A., Bottalico A., 2002. Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. European Journal of Plant Pathology 108: 597-609.
36. Lumsden R.D., Lewis J.A., Fravel D.R., 1995. Formulation and delivery of biocontrol agents for use against soilborne plant pathogens. In: Biorational Pest Control Agents, pp. 166-182. ACS Symposium Series. American Chemical Society, Washington DC, USA.
37. Marasas W.F.O., 1995. Fumonisins: their implications for human and animal health. Nature Toxins 3: 193-198.
38. Matsui K., 2006. Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Current Opinions in Plant Biology 9: 274-280.
39. Mazzoni E., Scandolara A., Giorni P., Pietri A., Battilani P., 2011. Field control of Fusarium ear rot Ostrinia nubilalis (Hübner), and fumonisins in maize kernels. Pest and Management Science 67: 458-465.
40. Miller J.D., 2001. Factors that affect the occurrence of fumonisin. Environmental Health Perspective. 109: 321-324.
41. Morris S.W., Vernooij B., Titatarn S., Starrett M., Thomas S., Wiltse C.C., Frederiksen R.A., Bhandhufalck A., Hulbert S., Uknes S., 1998. Induced resistance responses in maize. Molecular Plant Microbe Interactions 11: 643-658.
42. Mulè G., Susca A., Stea G., Moretti A., 2004. A species-specific PCR assay based on the calmodulin partial gene for identification of Fusarium verticillioides F. proliferatum and F. subglutinans. European Journal of Plant Pathology 110: 495-502.
43. Muller P.Y., Janovjak H., Miserez A., Dobbie Z., 2002. Processing of gene expression data generated by quantitative realtime RT-PCR. Biotechniques 32: 1372-1379.
44. Munkvold G.P., McGee D.C., Carlton W.M., 1997. Importance of different pathways for maize kernel infection by Fusarium moniliforme. Phytopathology 87: 209-217.
45. Nakamura S., Hatanaka A., 2002. Green-leaf-derived C6-aroma compounds with potent antibacterial action that act on both Gram-negative and Gram-positive bacteria. Journal of Agricultural and Food Chemistry 50: 7639-7644.
46. Nelson P.E., 1992. Taxonomy and biology of Fusarium moniliforme. Mycopathologia 117: 29-36.
47. Nemchenko A., Kunze S., Feussner I., Kolomiets M., 2006. Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm cold stress wounding pathogen infection and hormonal treatments. Journal of Experimental Botany 57: 3767-3779.
48. Ongena M., Duby F., Rossignol F., Fauconnier M.L., Dommes J., Thonart P., 2004. Stimulation of the lipoxygenase pathway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Molecular Plant-Microbe Interactions 17: 1009-1018.
49. Park Y.S., Kunze S., Ni X., Feussner I., Kolomiets M.V., 2010. Comparative molecular and biochemical characterization of segmentally duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta 231, 1425-1437.
50. Pfaffl M.W., 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: e45-e45.
51. Pieterse C.M.J., Schaller A., Mauch-Mani B., Conrath U., 2006. Signaling in plant resistance responses: divergence and cross-talk of defense pathways. In: Tuzun S., Bent E. (eds). Multigenic and Induced Systemic Resistance in Plants, pp. 166-196. Springer US. New York, NY, USA.
52. Placinta C., D'Mello J.P., Macdonald A.M., 1999. A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins. Animal Feed and Science Technology 78: 21-37.
53. Prelusky D.B., Rotter B.A., Rotter R.G., 1994. Toxicology of mycotoxins. In: Miller J.D., Trenholm H.L. (eds). Mycotoxins in Grain: Compounds Other than Aflatoxin, pp. 359-403. Eagan Press, St. Paul, MN, USA.
54. Ribnicky D.M., Shulaev V., Raskin I., 1998. Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiology 118: 565-572.
55. Rossi V., Battilani P., Battisti D., Scandolara A., 2004. Epidemiological aspects of Fusarium verticillioides the causal agent of maize pink ear rot. Journal of Plant Pathology 86: 331.
56. Rozen S., Skaletsky H., 1999. Primer3 on the WWW for general users and for biologist programmers in: Misener S., Krawetz S.A. (eds). Bioinformatics Methods and Protocols Methods in Molecular BiologyTM, pp. 365-386. Humana Press, Totowa, NJ, USA
57. Saldajeno M.G.B., Chandanie W.A., Kubota M., Hyakumachi M., 2008. Effects of interactions of arbuscular mycorrhizal fungi and beneficial saprophytic mycoflora on plant growth and disease protection. In: Siddiqui Z.A., Akhtar M.S., Futai K. (eds). Mycorrhizae: Sustainable Agriculture and Forestry, pp. 211-226. Springer, The Netherlands.
58. Sambrook J., Russell W.D., 2001. Molecular Cloning: a Laboratory Manual. CSHL Press Woodbury, NY, USA.
59. 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.
60. Shah J., 2009. Plants under attack: systemic signals in defense. Current Opinions in Plant Biology 12: 459-464.
61. 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. Phytopathology 95: 76-84.
62. 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 Physiology 147: 2147-2163.
63. Sobek E.A., Munkvold G.P., 1999. European corn borer (lepidoptera: pyralidae) larvae as vectors of Fusarium moniliforme causing kernel rot and symptomless infection of maize kernels. Journal of Economical Entomology 92: 503-509.
64. Sobowale A.A., Cardwell K.F., Odebode A.C., Bandyopadhyay R., Jonathan S.G., 2007. Persistence of Trichoderma species within maize stem against Fusarium verticillioides. Archives of Phytopathology and Plant Protection 40: 215-231.
65. Tuite J., 1969. Plant Pathological Methods. Fungi and Bacteria. Burgess Publishing Company. Minneapolis, MN, USA.
66. Vainio H., Heseltine E., Wilbourn J., 1993. Report on an IARC working group meeting on some naturally occurring substances. Internationl Journal of Cancer 53: 535-537.
67. Van Loon L.C., Bakker P.A.H.M., Pieterse C.M.J., 1998. Systemic resistance induced by rhizosphere bacteria. Annuual Review of Phytopathology 36: 453-483.
68. 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. Physiology and Molecular Plant Pathology 72: 80-86.
69. Wicklow D.T., Horn B.W., Shotwell O.L., Hesseltine C.W., Caldwell R.W., 1988. Fungal interference with Aspergillus flavus infection and aflatoxin contamination of maize grown in a controlled environment. Phytopathology 78: 68-74.
70. 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.
71. Yalpani N., Leon J., Lawton M.A., Raskin I., 1993. Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiology 103: 315-321.
72. Yates I.E., Bacon C.W., Hinton D.M., 1997. Effects of endophytic infection by Fusarium moniliforme on corn growth and cellular morphology. Plant Disease 81: 723-728.
73. Yedidia I., Benhamou N., Chet I., 1999. Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Applied and Environmental Microbiology 65: 1061-1070.
74. Yedidia I., Srivastva A.K., Kapulnik Y., Chet I., 2001. Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil 235: 235-242.
75. 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. Applied and Environmental Microbiology 69: 7343-7353.
76. Zimand G., Elad Y., Chet I., 1996. Effect of Trichoderma harzianum on Botrytis cinerea pathogenicity. Phytopathology 86: 1255-1260.