Effects of trichothecene production on the plant defense response and fungal physiology: Overexpression of the Trichoderma arundinaceum tri4 gene in T. harzianum

Applied and Environmental Microbiology

Volumn 81, Issue 18, 2015, Pages 6355-6366

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

^a UNIVERSITY OF LEÓN   (Spain)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; GENES; HYDROCARBON REFINING; PLANTS (BOTANY); PURIFICATION;

BIOACTIVE PROPERTIES; CYTOTOXIC ACTIVITIES; DEFENSE RELATED GENES; PHYTOTOXIC ACTIVITY; PLANT DEFENSE RESPONSE; ROOT COLONIZATION; SESQUITERPENOIDS; STRUCTURAL COMPLEXITY;

GENE EXPRESSION;

ANTAGONISM; ANTIMICROBIAL ACTIVITY; BIOACTIVITY; ERGOSTEROL; FUNGUS; GENE EXPRESSION; HOST PLANT; PHYSIOLOGY; PHYTOTOXICITY; PLANT DEFENSE; ROOT COLONIZATION; TOXIN;

ANIMALIA; FUSARIUM; LYCOPERSICON ESCULENTUM; TRICHODERMA; TRICHODERMA BREVICOMPACTUM;

12,13-EPOXYTRICHOTHEC-9-ENE; ANTIFUNGAL AGENT; CYCLOHEXENE DERIVATIVE; ERGOSTEROL; HARZIANUM A; SESQUITERPENE; SQUALENE; TRICHODERMIN; TRICHODIENE; TRICHOTHECENE DERIVATIVE;

BIOSYNTHESIS; CHEMISTRY; DOWN REGULATION; DRUG EFFECTS; FUNGAL GENE; FUSARIUM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGY; TOMATO; TRICHODERMA;

ANTIFUNGAL AGENTS; CYCLOHEXENES; DOWN-REGULATION; ERGOSTEROL; FUSARIUM; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; LYCOPERSICON ESCULENTUM; MUTATION; SESQUITERPENES; SQUALENE; TRICHODERMA; TRICHODERMIN; TRICHOTHECENES;

EID: 84945260368     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01626-15     Document Type: Article

References (44)

1. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 2004. Trichoderma species- opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43-56. http://dx.doi.org/10.1038/nrmicro797.
2. Lorito M, Woo SL, Harman GE, Monte E. 2010. Translational research on Trichoderma: from 'omics to the field. Annu Rev Phytopathol 48:395- 417. http://dx.doi.org/10.1146/annurev-phyto-073009-114314.
3. Shoresh M, Harman GE, Mastouri F. 2010. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21-43. http://dx.doi.org/10.1146/annurev-phyto-073009-114450.
4. Hermosa R, Viterbo A, Chet I, Monte E. 2012. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17-25. http://dx.doi.org /10.1099/mic.0.052274-0.
5. Alexander NJ, McCormick SP, Zeigenhorn SL. 1999. Phytotoxicity of selected trichothecenes using Chlamydomonas reinhardtii as a model system. Nat Toxins 7:265-269. http://dx.doi.org/10.1002/1522-7189(199911 /12)7:6<265::AID-NT65>3.0.CO;2-5.
6. Desjardins AE, McCormick SP, Appell M. 2007. Structure-activity relationships of trichothecene toxins in an Arabidopsis thaliana leaf assay. J Agric Food Chem 55:6487-6492. http://dx.doi.org/10.1021/jf0709193.
7. Bondy GS, McCormick SP, Beremand MN, Pestka JJ. 1991. Murine lymphocyte proliferation impaired by substituted neosolaniols and calonectrins-Fusarium metabolites associated with trichothecene biosynthesis. Toxicon 29:1107-1113. http://dx.doi.org/10.1016/0041-0101 (91)90208-9.
8. Hohn TM, Beremand PD. 1989. Isolation and nucleotide sequence of a sesquiterpene cyclase gene from the trichothecene-producing fungus Fusarium sporotrichioides. Gene 79:131-138. http://dx.doi.org/10.1016/0378 -1119(89)90098-X.
9. Cardoza RE, Malmierca MG, Hermosa MR, Alexander NJ, McCormick SP, Proctor RH, Tijerino AM, Rumbero A, Monte E, Gutiérrez S. 2011. Identification of loci and functional characterization of trichothecene biosynthetic genes in the filamentous fungus Trichoderma. Appl Environ Microbiol 77:4867-4877. http://dx.doi.org/10.1128/AEM.00595-11.
10. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Hermosa R, Monte E, Gutiérrez S. 2012. Involvement of Trichoderma trichothecenes in the biocontrol activity and in the induction of plant defenserelated genes. Appl Environ Microbiol 78:4856-4868. http://dx.doi.org /10.1128/AEM.00385-12.
11. Godtfredsen WO, Vangedal S. 1965. Trichodermin, a new sesquiterpene antibiotic. Acta Chem Scand 19:1088-1102. http://dx.doi.org/10.3891 /acta.chem.scand.19-1088.
12. Corley DG, Miller-Wideman M, Durley RC. 1994. Isolation and structure of harzianum A: a new trichothecene from Trichoderma harzianum. J Nat Prod 57:422-425. http://dx.doi.org/10.1021/np50105a019.
13. Nielsen KF, Gräfenhan T, Zafari D, Thrane U. 2005. Trichothecene production by Trichoderma brevicompactum. J Agric Food Chem 53: 8190-8196. http://dx.doi.org/10.1021/jf051279b.
14. Rocha O, Ansari K, Doohan FM. 2005. Effects of trichothecene mycotoxins on eukaryotic cells: a review. Food Addit Contam 22:369-378. http: //dx.doi.org/10.1080/02652030500058403.
15. Jin HZ, Lee JH, Zhang WD, Lee HB, Hong YS, Kim YH, Lee JJ. 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. http://dx.doi.org/10.1080/10286020500531977.
16. Degenkolb T, Dieckmann R, Nielsen KF, Gräfenhan T, Theis C, Zafari D, Chaverri P, Isamaiel A, Brückner H, von Döhren H, Thrane U, Petrine O, Samuels GJ. 2008. The Trichoderma brevicompactum clade: a separate lineage with new species, new peptabiotics, and mycotoxins. Mycol Prog 7:177-219. http://dx.doi.org/10.1007/s11557-008-0563-3.
17. Lee HB, Kim Y, Jin HZ, Lee JJ, Kin C-J, Park JY, Jung HS. 2005. A new Hypocrea strain producing harzianum A cytotoxic to tumour cell lines. Lett Appl Microbiol 40:497-503. http://dx.doi.org/10.1111/j.1472-765X .2005.01719.x.
18. Wu Q, Dohnal V, Kuca K, Yuan Z. 2013. Trichothecenes: structure-toxic activity relationships. Curr Drug Metab 14:641-660. http://dx.doi.org/10 .2174/1389200211314060002.
19. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Collado IG, Hermosa MR, Monte E, Gutiérrez S. 2013. Relevance of trichothecenes in fungal physiology: disruption of tri5 in Trichoderma arundinaceum. Fungal Genet Biol 53:22-33. http://dx.doi.org/10.1016/j.fgb.2013 .02.001.
20. Malmierca MG, McCormick SP, Cardoza RE, Alexander NJ, Monte E, Gutiérrez S. 12 May 2014. Production of trichodiene by Trichoderma harzianum alters the perception of this biocontrol strain by plants and antagonized fungi. Environ Microbiol http://dx.doi.org/10.1111/1462 -2920.12506.
21. Quidde T, Osbourn AE, Tudzynski P. 1998. Detoxification of α-tomatine by Botrytis cinerea. Physiol Mol Plant Pathol 52:151-165. http://dx .doi.org/10.1006/pmpp.1998.0142.
22. Penttilä M, Nevalainen H, Ratto M, Salminen E, Knowles J. 1987. A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene 61:155-164. http://dx.doi.org/10.1016/0378 -1119(87)90110-7.
23. Ghimire GP, Lee HC, Sohng JK. 2009. Improved squalene production via modulation of the methylerythritol 4-phosphate pathway and heterologous expression of genes from Streptomyces peucetius ATCC 27952 in Escherichia coli. Appl Environ Microbiol 75:7291-7293. http://dx.doi.org /10.1128/AEM.01402-09.
24. Cardoza RE, Hermosa MR, Vizcaíno JA, González FJ, Llobell A, Monte E, Gutiérrez S. 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. http://dx.doi.org/10.1016/j.fgb.2006.11 .013.
25. Ausubel FM, Brent R, Kingston RE, Moore DJ, Smith A, Seidman JG, Struhl K. 1987. Current protocols in molecular biology. Wiley, New York, NY.
26. Gutiérrez S, Velasco J, Marcos AT, Fernández FJ, Fierro F, Barredo JL, Díez B, Martín JF. 1997. Expression of the cefG gene is limiting for cephalosporin biosynthesis in Acremonium chrysogenum as shown by promoter replacement studies. Appl Microbiol Biotechnol 48:606-614. http: //dx.doi.org/10.1007/s002530051103.
27. Cardoza RE, Vizcaíno JA, Hermosa R, Monte E, Gutiérrez S. 2006. A comparison of the phenotypic and genetic stability of recombinant Trichoderma spp. generated by protoplast- and Agrobacterium-mediated transformation. J Microbiol 44:383-395.
28. Hohn TM, Desjardings AE, McCormick SP. 1995. The tri4 of Fusarium sporotrichioides encodes a cytochrome P450 monooxygenase involved in trichothecene biosynthesis. Mol Gen Genet 248:95-102. http://dx.doi.org /10.1007/BF02456618.
29. Trapp SC, 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. http://dx.doi.org/10 .1007/s004380050666.
30. 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. http://dx.doi.org/10.1099/mic.0.052118-0.
31. Cardoza RE, Malmierca MG, Gutiérrez S. 2014. Overexpression of erg1 gene in Trichoderma harzianum CECT 2413: effect on the induction of tomato defence-related genes. J Appl Microbiol 117:812-823. http://dx .doi.org/10.1111/jam.12574.
32. Malmierca MG, Barua J, McCormick SP, Izquierdo-Bueno I, Cardoza RE, Alexander NJ, Hermosa R, Collado IG, Monte E, Gutiérrez S. 2015. Novel aspinolide production by Trichoderma arundinaceum with a potential role in Botrytis cinerea antagonistic activity and plant defence priming. Environ Microbiol 17:1103-1118. http://dx.doi.org/10.1111/1462-2920 .12514.
33. Pinedo C, Wang CM, Pradier JM, Dalmais B, Choquer M, Le Pecheur P, Morgant G, Collado IG, Cane DE, Viaud M. 2008. Sesquiterpene synthase from the botrydial biosynthetic gene cluster of the phytopathogen Botrytis cinerea. ACS Chem Biol 3:791-801. http://dx.doi.org/10.1021 /cb800225v.
34. 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. http://dx.doi.org/10.1111/j.1364 -3703.2010.00674.x.
35. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034.
36. 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. http://dx .doi.org/10.1093/nar/30.9.e36.
37. Pilsyk S, Perlinska-Lenart U, Gorka-Niec W, Graczyk S, Antosiewicz B, Zembek P, Palamarczyk G, Kruszewska JS. 2014. Overexpression of erg20 gene encoding farnesyl pyrophosphate synthase has contrasting effects on activity of enzymes of the dolichyl and sterol branches of mevalonate pathway in Trichoderma reesei. Gene 544:114-122. http://dx.doi.org /10.1016/j.gene.2014.04.073.
38. Paradise EM, Kirby J, Chan R, Keasling JD. 2008. Redirection of flux through the FPP branch-point in Saccharomyces cerevisiae by downregulating squalene synthase. Biotechnol Bioeng 100:371-378. http://dx .doi.org/10.1002/bit.21766.
39. Veen M, Stahl U, Lang C. 2003. Combined overexpression of genes of the ergosterol biosynthetic pathway leads to accumulation of sterols in Saccharomyces cerevisiae. FEMS Yeast Res 4:87-95. http://dx.doi.org/10.1016 /S1567-1356(03)00126-0.
40. Alonso-Ramírez A, Poveda J, Martin I, Hermosa R, Monte E, Nicolás C. 2014. Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots. Mol Plant Pathol 15:823-831. http://dx.doi.org /10.1111/mpp.12141.
41. León-Morcillo RJ, Martín-Rodríguez M-R, Vierheilig H, Ocampo JA, García-Garrido JM. 2012. Late activation of the 9-oxylipin pathway during arbuscular mycorrhiza formation in tomato and its regulation by jasmonate signalling. J Exp Bot 63:3545-3558. http://dx.doi.org/10.1093/jxb /ers010.
42. Harel Y, Mehari ZH, Rav-David D, Elad Y. 2014. Systemic resistance to gray mold induced in tomato by benzothiadiazole and Trichoderma harzianum T39. Phytopathology 104:150-157. http://dx.doi.org/10.1094 /PHYTO-02-13-0043-R.
43. Iqbal N, Teivellini A, Masood A, Ferrante A, Khan NA. 2013. Current understanding on ethylene signaling in plants: the influence of nutrient availability. Plant Physiol Biochem 73:128-138. http://dx.doi.org/10.1016 /j.plaphy.2013.09.011.
44. Hermosa R, Rubio MB, Cardoza RE, Nicolás C, Monte E, Gutiérrez S. 2013. The contribution of Trichoderma to balancing the costs of plant growth and defence. Int Microbiol 16:69-80.