Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes

Applied and Environmental Microbiology

Volumn 78, Issue 14, 2012, Pages 4856-4868

  Malmierca, M G ^a   Cardoza, R E ^a   Alexander, N J ^b   McCormick, S P ^b   Hermosa, R ^c   Monte, E ^c   Gutierrez S ^a  

^a UNIVERSITY OF LEÓN   (Spain)

^b NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

^c UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-FUNGAL ACTIVITY; BIOSYNTHETIC PATHWAY; BOTRYTIS CINEREA; CYTOCHROME P450; DEFENSE RELATED GENES; FUNGAL PATHOGEN; FUSARIUM; GENE DISRUPTIONS; GENES ENCODING; GENOMIC ORGANIZATION; JASMONATES; MONOOXYGENASES; ORTHOLOGUES; R. SOLANI; RHIZOCTONIA SOLANI; SALICYLIC ACIDS; TOMATO PLANTS; TOMATO SEEDLINGS; TRANSFORMANTS; TRICHODERMA; TRICHOTHECENES; WILD-TYPE STRAIN;

BIOCONTROL; FRUITS; GENE ENCODING; PLANT CELL CULTURE; PLANTS (BOTANY);

GENE EXPRESSION;

ANTIFUNGAL AGENT; CYTOCHROME P450; FUNGAL PROTEIN; TRICHOTHECENE DERIVATIVE;

ANTIMICROBIAL ACTIVITY; BIOCONTROL AGENT; BIOLOGICAL CONTROL; FRUIT; FUNGUS; GENE EXPRESSION; GENOMICS; HOST PLANT; HOST-PATHOGEN INTERACTION; PLANT DEFENSE; PROTEIN; SEEDLING;

ARTICLE; BIOLOGICAL PEST CONTROL; BOTRYTIS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HYPHOMYCETES; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PLANT DISEASE; PLANT GENE; TOMATO; TRICHODERMA;

ANTIFUNGAL AGENTS; BOTRYTIS; CYTOCHROME P-450 ENZYME SYSTEM; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; LYCOPERSICON ESCULENTUM; PEST CONTROL, BIOLOGICAL; PLANT DISEASES; RHIZOCTONIA; TRICHODERMA; TRICHOTHECENES;

BOTRYOTINIA FUCKELIANA; FUSARIUM; LYCOPERSICON ESCULENTUM; THANATEPHORUS CUCUMERIS; TRICHODERMA;

EID: 84863758012     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00385-12     Document Type: Article

References (59)

1. Ahn IP, Lee SW, Suh SC. 2007. Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol. Plant Microbe Interact. 20:759-768.
2. Alexander NJ, Hohn TH, McCormick SP. 1998. The TRI11 gene of Fusarium sporotrichioides encodes a cytochrome P-450 monooxygenase required for C-15 hydroxylation in trichothecene biosynthesis. Appl. Environ. Microbiol. 64:221-225.
3. Alexander NJ, McCormick SP, Blackburn JA. 2008. Effects of xanthotoxin treatment on trichothecene production in Fusarium sporotrichioides. Can. J. Microbiol. 54:1023-1031.
4. Ausubel FM, et al (ed). 1987. Current protocols in molecular biology. John Wiley & Sons, Inc, New York, NY.
5. Baldwin C, Bycroft BW, Dewick PM, Gilbert J, Holden I. 1985. Biosynthesis of trichothecene mycotoxins in Fusarium culmorum cultures. Z. Naturforsch. C 40:514-518.
6. Benítez T, Rincón AM, Limón MC, Codón AC. 2004. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7:249-260.
7. Bennett JW, Klich M. 2003. Mycotoxins. Clin. Microbiol. Rev. 16:497-516.
8. Brown DW, McCormick SP, Alexander NJ, Proctor RH, Desjardins AE. 2001.Agenetic and biochemical approach to study trichothecene diversity in Fusarium sporotrichioides and Fusarium graminearum. Fungal Genet. Biol. 32:121-133.
9. Cardoza RE, Vizcaíno JA, Hermosa R, Monte E, Gutiérrez S. 2006. A comparison on the phenotypic and genetic stability of the recombinant Trichoderma spp. generated by protoplast- and Agrobacterium-mediated transformation. J. Microbiol. 44:383-395.
10. Cardoza RE, et al. 2007. Partial silencing of a hydroxy-methylglutaryl-CoA reductase encoding gene in Trichoderma harzianum CECT 2413 results in a lower level of resistance to lovastatin and a lower antifungal activity. Fungal Genet. Biol. 44:269-283.
11. Cardoza RE, et al. 2011. Identification of loci and functional characterization of trichothecene biosynthetic genes in the filamentous fungus Trichoderma. Appl. Environ. Microbiol. 77:4867-4877.
12. Cole RA, Jarvis BB, Schweikert MA (ed). 2003. Handbook of secondary fungal metabolites, vol III, p 199-560. Academic Press, San Diego, CA.
13. Conrath U, et al. 2006. Priming: getting ready for battle. Mol. Plant Microbe Interact. 19:1062-1071.
14. Degenkolb T, et al. 2008. The Trichoderma brevicompactum clade: a separate lineage with new species, new peptabiotics, and mycotoxins. Mycol. Prog. 7:177-219.
15. De Groot MJ, Bundock P, Hooykaas PJ, Beijersbergen AG. 1998. Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nat. Biotechnol. 16:839-842.
16. Desjardins AE. 2006. Fusarium mycotoxins. Chemistry, genetics and biology. American Phytopathological Society, St. Paul, MN.
17. Elad Y. 2000. Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Prot. 19: 709-714.
18. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 2004. Trichoderma species- opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2:43-56.
19. Harman GE, Petzoldt R, Comis A, Chen J. 2004. Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and ef-fects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology 94:147-153.
20. Harman GE. 2006. Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190-194.
21. Hermosa R, Viterbo A, Chet I, Monte E. 2012. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17-25.
22. Hesketh AR, et al. 1990. Isotrichodiol: a post-trichodiene intermediate in the biosynthesis of trichothecene mycotoxins. J. Chem. Soc. Chem. Commun. (Camb.) 17:1184-1186.
23. Hesketh AR, et al. 1991. Biosynthesis of trichothecene mycotoxins: identification of isotrichodiol as a post-trichodiene intermediate. Phytochemistry 30:2237-2243.
24. Hohn TM, Beremand P. 1989. Isolation and nucleotide sequence of a sesquiterpene cyclase gene from the trichothecene-producing fungus Fusarium sporotrichioides. Gene 79:131-138.
25. Hohn TM, VanMiddlesworth F. 1986. Purification and characterization of the sesquiterpene cyclase trichodiene synthetase from Fusarium sporotrichioides. Arch. Biochem. Biophys. 251:756-761.
26. Hohn TM, McCormick SP, Desjardins AE. 1993. Evidence for a gene cluster involving trichothecene-pathway biosynthetic genes in Fusarium sporotrichioides. Curr. Genet. 24:291-295.
27. Hohn TM, Desjardins AE, McCormick SP. 1995. The Tri4 gene of Fusarium sporotrichioides encodes a cytochrome P450 monooxygenase involved in trichothecene biosynthesis. Mol. Gen. Genet. 248:95-102.
28. Jin H-Z, et al. 2007. Harzianums A and B produced by a fungal strain, Hypocrea sp. F000527, and their cytotoxicity against tumor cell lines. J. Asian Nat. Prod. Res. 9:203-207.
29. Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M. 2007. Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes and evolution. Biosci. Biotechnol. Biochem. 71:2105-2123.
30. Lee HB, et al. 2005. A new Hypocrea strain producing harzianum A cytotoxic to tumour cell lines. Lett. Appl. Microbiol. 40:497-503.
31. Lorito M, Woo SL, Harman GE, Monte E. 2010. Translational research on Trichoderma: from 'omics to the field. Annu. Rev. Phytopathol. 48: 395-417.
32. Lutz MP, Feichtinger G, Défago G, Brion D. 2003. Mycotoxigenic Fusarium and deoxynivalenol production repress chitinase gene expression in the biocontrol agent Trichoderma atroviride P1. Appl. Environ. Microbiol. 69:3077-3084.
33. Machida Y, Nozoe S. 1972. Biosynthesis of trichothecin and related compounds. Tetrahedron 28:5113-5117.
34. McCormick SP, Taylor SL, Plattner RD, Beremand MN. 1989. New modified trichothecenes accumulated in solid culture by mutant strains of Fusarium sporotrichioides. Appl. Environ. Microbiol. 55:2195-2199.
35. McCormick SP, Hohn TM, Desjardins AE. 1996. Isolation and characterization of Tri3, a gene encoding 15-O-acetyltransferase from Fusarium sporotrichioides. Appl. Environ. Microbiol. 62:353-359.
36. McCormick SP, Alexander NJ, Proctor RH. 2006. Fusarium tri4 encodes a multifunctional oxygenase required for trichothecene biosynthesis. Can. J. Microbiol. 52:636-642.
37. McCormick SP, Alexander NJ. 2007. Myrothecium roridum tri4 encodes a multifunctional oxygenase required for three oxygenation steps. Can. J. Microbiol. 53:572-579.
38. McCormick SP, Alexander NJ, Harris LJ. 2010. CLM1 of Fusarium graminearum encodes a longiborneol synthase required for culmorin production. Appl. Environ. Microbiol. 76:136-141.
39. McCormick SP, Stanley AM, Stover NA, Alexander NJ. 2011. Trichothecenes: from simple to complex mycotoxins. Toxins (Basel) 3:802-814.
40. Pfaffl MW, Horgan GW, Dempfle L. 2002. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30:e36. doi: 10.1093/nar/30.9.e36.
41. Price MS, et al. 2006. The aflatoxin pathway regulator AflR induces gene transcription inside and outside of the aflatoxin biosynthetic cluster. FEMS Microbiol. Lett. 255:275-279.
42. Proctor RH, Hohn TM, McCormick SP, Desjardins AE. 1995. Tri6 encodes an unusual zinc finger protein involved in regulation of trichothecene biosynthesis in Fusarium sporotrichioides. Appl. Environ. Microbiol. 61:1923-1930.
43. Proctor RH, McCormick SP, Alexander NJ, Desjardins AE. 2009. Evidence that a secondary metabolic biosynthetic gene cluster has grown by gene relocation during evolution of the filamentous fungus Fusarium. Mol. Microbiol. 74:1128-1142.
44. Rodrígues P, Venancio A, Kozakiewicz Z, Lima N. 2009. A polyphasic approach to the identification of aflatoxigenic and non-aflatoxigenic strains of Aspergillus section Flavi isolated from Portuguese almonds. Int. J. Food Microbiol. 129:187-193.
45. Rubio MB, Domínguez S, Monte E, Hermosa R. 2012. Comparative study of Trichoderma gene expression in interactions with tomato plants using high-density oligonucleotide microarrays. Microbiology 158:119-128.
46. Sevim A, et al. 2012. Hydrophobin genes of the entomopathogenic fungus, Metarhizium brunneum, are differentially expressed and corresponding mutants are decreased in virulence. Curr. Genet. 58:79-92.
47. Shoresh M, Harman GE, Mastouri F. 2010. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 48:21-43.
48. Sivasithamparam K, Ghisalberti EL. 1998. Secondary metabolism in Trichoderma and Gliocladium, p 139-191. In Kubicek CP, Harman GE (ed), Trichoderma and Gliocladium, vol I. Taylor & Francis, London, England.
49. Sousa S. 2004. Mejora del sistema de expresión en Trichoderma harzianum CECT 2413 para la producción de proteínas de interés biotecnológico. Ph.D. thesis. University of Sevilla, Seville, Spain.
50. Tijerino A, et al. 2011. Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet. Biol. 48:285-296.
51. Tokai T, et al. 2005. Screening of putative oxygenase genes in the Fusarium graminearum genome sequence database for their role in trichothecene biosynthesis. FEMS Microbiol. Lett. 251:193-201.
52. Tokai T, et al. 2007. Fusarium Tri4 encodes a key multifunctional cytochrome P450 monooxygenase for four consecutive oxygenation steps in trichothecene biosynthesis. Biochem. Biophys. Res. Commun. 353:412-417.
53. Trapp SE, Hohn TM, McCormick SP, Jarvis BB. 1998. Characterization of the gene cluster for biosynthesis of macrocyclic trichothecenes in Myrothecium roridum. Mol. Gen. Genet. 257:421-432.
54. 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.
55. Turgeon BG, Garber RC, Yoder OC. 1987. Development of a fungal transformation system based on selection of sequences with promoter activity. Mol. Cell. Biol. 17:3297-3305.
56. Vandesompele J, et al. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:0034.1-0034.11. doi:10.1186/gb-2002-3-7-research0034.
57. Vinale F, et al. 2008. Trichoderma-plant-pathogen interactions. Soil Biol. Biochem. 40:1-10.
58. Werck-Reichhart D, Feyereisen R. 2000. Cytochromes P450: a success story. Genome Biol. 1:3003.1-3003.9. doi:10.1186/gb-2000-1-6-reviews3003.
59. Zamir LO, Devor KA, Sauriol F. 1991. Biosynthesis of the trichothecene 3-acetyldeoxynivalenol. Identification of the oxygenation steps after isotrichodermin. J. Biol. Chem. 266:14992-15000.