Altered trichothecene biosynthesis in TRI6-silenced transformants of Fusarium culmorum influences the severity of crown and foot rot on durum wheat seedlings

Molecular Plant Pathology

Volumn 12, Issue 8, 2011, Pages 759-771

  Scherm, Barbara ^a   Orrù, Marcella ^a   Balmas, Virgilio ^a   Spanu, Francesca ^a   Azara, Emanuela ^b   Delogu, Giovanna ^b   Hammond, Thomas M ^c   Keller, Nancy P ^d   Migheli, Quirico ^a  

^a UNIVERSITY OF SASSARI   (Italy)

^b CNR Consiglio Nazionale delle Ricerche   (Italy)

^c UNIVERSITY OF MISSOURI   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; TRANSCRIPTION FACTOR; TRICHOTHECENE DERIVATIVE;

ARTICLE; BIOSYNTHESIS; FUSARIUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; NORTHERN BLOTTING; PATHOGENICITY; PHYSIOLOGY; VIRULENCE; WHEAT;

BLOTTING, NORTHERN; FUNGAL PROTEINS; FUSARIUM; GENE EXPRESSION REGULATION, FUNGAL; TRANSCRIPTION FACTORS; TRICHOTHECENES; TRITICUM; VIRULENCE;

BACTERIA (MICROORGANISMS); FUNGI; FUSARIUM CULMORUM; TRITICUM AESTIVUM; TRITICUM TURGIDUM SUBSP. DURUM;

EID: 80052416030     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2011.00709.x     Document Type: Article

References (53)

1. Aleandri, M.P., Magro, P. and Chilosi, G. (2007) Modulation of host pH during the wheat-Fusarium culmorum interaction and its influence on the production and activity of pectolytic enzymes. Plant Pathol. 56, 517-525.
2. Alexander, N.J., Hohn, T.M. and McCormick, S.P. (1998) The Tri111 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, N.J., Proctor, R.H. and McCormick, S.P. (2009) Genes, gene clusters, and biosynthesis of trichothecenes and fumonisins in Fusarium. Toxin Rev. 28, 198-215.
4. Bai, G.H., Desjardins, A.E. and Plattner, R.D. (2002) Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia, 15, 91-98.
5. Bottalico, A. and Perrone, G. (2002) Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur. J. Plant Pathol. 108, 611-624.
6. Boutigny, A.L., Richard-Forget, F. and Barreau, C. (2008) Natural mechanisms for cereal resistance to the accumulation of Fusarium trichothecenes. Eur. J. Plant Pathol. 121, 411-423.
7. Boutigny, A.L., Barreau, C., Atanasova-Penichon, V., Verdal-Bonnin, M.N., Pinson-Gadais, L. and Richard-Forget, F. (2009) Ferulic acid, an efficient inhibitor of type B trichothecene biosynthesis and Tri gene expression in Fusarium liquid cultures. Mycol. Res. 113, 746-753.
8. Cariddi, C. and Catalano, M. (1990) Water stress and Fusarium culmorum infections on durum wheat. Phytopathol. Mediterr. 29, 51-55.
9. Catalanotto, C., Azzalin, G., Macino, G. and Cogoni, C. (2000) Transcription: gene silencing in worms and fungi. Nature, 404, 245.
10. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 56-59.
11. Cogoni, C. (2001) Homology-dependent gene silencing mechanisms in fungi. Annu. Rev. Microbiol. 55, 381-406.
12. Cogoni, C. and Macino, G. (1997) Conservation of transgene-induced post-transcriptional gene silencing in plants and fungi. Trends Plant Sci. 2, 438-443.
13. Corazza, L., Balmas, V., Santori, A., Vitale, S., Luongo, L. and Maccaroni, M. (2002) Head blight and foot rot of wheat in Italy. Petria, 12, 25-36.
14. Cotty, P.J., Antilla, L. and Wakelyn, P.J. (2007) Competitive exclusion of aflatoxin producers: farmer driven research and development. In: Biological Control: A Global Perspective (Vincent, C., Goettel, M.S. and Lazarovits, G., eds), pp. 241-253. Wallingford, Oxfordshire: CABI.
15. Denli, A.M. and Hannon, G.J. (2003) RNAi: an ever-growing puzzle. Trends Biochem. Sci. 28, 196-201.
16. Desjardins, A.E., Hohn, T.M. and McCormick, S.P. (1993) Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol. Rev. 57, 596-604.
17. Desjardins, A.E., Proctor, R.H., Bai, G., McCormick, S.P., Shaner, G., Buechley, G. and Hohn, T.M. (1996) Reduced virulence of trichothecene-nonproducing mutants of Gibberella zeae in wheat field tests. Mol. Plant-Microbe Interact. 9, 775-781.
18. Desjardins, A.E., Bai, G., Plattner, R.D. and Proctor, R.H. (2000) Analysis of aberrant virulence of Gibberella zeae following transformation-mediated complementation of a trichothecene-deficient (TRI5) mutant. Microbiology, 146, 2059-2068.
19. Desmond, O.J., Manners, J.M., Stephens, A.E., Maclean, D.J., Schenk, P.M., Gardiner, D.M., Munn, A.L. and Kazan, K. (2008) The Fusarium mycotoxin deoxynivalenol elicits hydrogen peroxide production, programmed cell death and defence responses in wheat. Mol. Plant Pathol. 9, 435-445.
20. Gardiner, D.M., Kazan, K. and Manners, J.M. (2009) Nutrient profiling reveals potent inducers of trichothecene biosynthesis in Fusarium graminearum. Fungal Genet. Biol. 46, 604-613.
21. Giobbe, S., Marceddu, S., Scherm, B., Zara, G., Mazzarello, V., Budroni, M. and Migheli, Q. (2007) The strange case of a biofilm-forming strain of Pichia fermentans, which controls Monilinia brown rot on apple but is pathogenic on peach fruit. FEMS Yeast Res. 7, 1389-1398.
22. Goswami, R.S. and Kistler, H.C. (2004) Heading for disaster: Fusarium graminearum on cereal rops. Mol. Plant Pathol. 5, 515-525.
23. Harris, L.J., Desjardins, A.E., Plattner, R.D., Nicholson, P., Butler, G., Young, J.C., Weston, G., Proctor, R.H. and Hohn, T.M. (1999) Possible role of trichothecene mycotoxins in virulence of Fusarium graminearum on maize. Plant Dis. 83, 954-960.
24. Henry, C., Mounya, I. and Latgé, J.P. (2007) Testing the efficacy of RNA interference constructs in Aspergillus fumigatus. Curr. Genet. 51, 277-284.
25. Hohn, T.M. and Beremand, P. (1989) Isolation and nucleotide sequence of a sesquiterpene cyclase gene from the trichothecene-producing fungus Fusarium sporotrichioides. Gene, 79, 131-138.
26. Hohn, T.M., Krishna, R. and Proctor, R.H. (1999) Characterization of a transcriptional activator controlling trichothecene toxin biosynthesis. Fungal Genet. Biol. 26, 224-235.
27. Hua-Van, A., Pamphile, J.A., Langin, T. and Daboussi, M.J. (2001) Transposition of autonomous and engineered impala transposons in Fusarium oxysporum and a related species. Mol. Gen. Genet. 264, 724-731.
28. Jansen, C., von Wettstein, D., Schäfer, W., Kogel, K.H., Felk, A. and Maier, F.J. (2005) Infection patterns in barley and wheat spikes inoculated with wild type and trichodiene synthase gene disrupted Fusarium graminearum. Proc. Natl. Acad. Sci. USA, 102, 16892-16897.
29. Kang, Z. and Buchenauer, H. (2002) Studies on the infection process of Fusarium culmorum in wheat spikes: degradation of host cell wall components and localization of trichothecene toxins in infected tissue. Eur. J. Plant Pathol. 108, 653-660.
30. Langin, T., Daboussi, M.J., Gerlinger, C. and Brygoo, Y. (1990) Influence of biological parameters and gene transfer technique on transformation of Fusarium oxysporum. Curr. Genet. 17, 313-319.
31. Maier, F.J., Miedaner, T., Hadeler, B., Felk, A., Salomon, S., Lemmens, M., Kassner, H. and Schäfer, W. (2006) Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Mol. Plant Pathol. 7, 449-461.
32. McCormick, S.P. (2003) The role of DON in pathogenicity. In: Fusarium Head Blight of Wheat and Barley (Leonard, K.J. and Bushnell, W.R., eds), pp. 165-183. St. Paul, MN: APS Press.
33. McDonald, T., Brown, D., Keller, N.P. and Hammond, T.M. (2005) RNA silencing of mycotoxin production in Aspergillus and Fusarium species. Mol. Plant-Microbe Interact. 18, 539-545.
34. McKinney, H.H. (1923) Influence of soil temperature and moisture on infection of wheat seedlings by Helminthosporium sativum. J. Agric. Res. 26, 195-217.
35. Migheli, Q., Friard, O., Del Tedesco, D., Musso, M.R. and Gullino, M.L. (1996) Stability of transformed antagonistic Fusarium oxysporum strains in vitro and in soil microcosms. Mol. Ecol. 5, 641-649.
36. Nakayashiki, H., Hanada, S., Nguyen, B.Q., Kadotani, N., Tosa, Y. and Mayama, S. (2005) RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet. Biol. 42, 275-283.
37. Nakayashiki, H. and Nguyen, Q.B. (2008) RNA interference: roles in fungal biology. Curr. Opin. Microbiol. 11, 494-502.
38. Pickford, A.S. and Cogoni, C. (2003) RNA-mediated gene silencing. Cell. Mol. Life Sci. 60, 871-882.
39. Proctor, R.H., Hohn, T.M., McCormick, S.P. and Desjardins, A.E. (1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene biosynthetic gene. Mol. Plant-Microbe Interact. 8, 593-601.
40. Proctor, R.H., Desjardins, A.E., McCormick, S.P., Plattner, N.J., Alexander, N.J. and Brown, D.W. (2002) Genetic analysis of the role of trichothecene and fumonisin mycotoxins in the virulence of Fusarium. Eur. J. Plant Pathol. 108, 691-698.
41. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning, A Laboratory Manual, 2nd edn. New York: Cold Spring Harbor Laboratory Press.
42. Smiley, R.W. and Patterson, L.M. (1996) Pathogenic fungi associated with Fusarium foot rot of winter wheat in the semiarid Pacific Northwest. Plant Dis. 80, 944-949.
43. Sudakin, D.L. (2003) Trichothecenes in the environment: relevance to human health. Toxicol. Lett. 143, 97-107.
44. Tanguay, P., Bozza, S. and Breuil, C. (2006) Assessing RNAi frequency and efficiency in Ophiostoma floccosum and O. piceae. Fungal Genet. Biol. 43, 804-812.
45. Vogel, H.J. (1956) A convenient growth medium for Neurospora (Medium N). Microb. Genet. Bull. 13, 42-43.
46. Wagacha, J.M. and Muthomi, J.W. (2007) Fusarium culmorum: infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat. Crop Prot. 26, 877-885.
47. Walker, N.J. (2002) A technique whose time has come. Science, 296, 557-559.
48. Ward, T.J., Clear, R.M., Rooney, A.P., O'Donnell, K., Gaba, D., Patrick, S., Starkey, D.E., Gilbert, J., Geiser, D.M. and Nowicki, T.W. (2008) An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet. Biol. 45, 473-484.
49. Waterhouse, P.M., Wang, M.B. and Lough, T. (2001) Gene silencing as an adaptive defence against viruses. Nature, 411, 834-842.
50. Wei, C.M. and McLaughlin, C.S. (1974) Structure-function relationship in the 12, 13-epoxytrichothecenes. Novel inhibitors of protein synthesis. Biochem. Biophys. Res. Commun. 57, 838-844.
51. Wiese, M.V. (1987) Compendium of Wheat Diseases. St. Paul, MN: APS Press.
52. Yang, G.H., Jarvis, B.B., Chung, Y.J. and Pestka, J.J. (2000) Apoptosis induction by the satratoxins and other trichothecene mycotoxins: relationship to ERK, p8 MAPK, and SAPK/JNK activation. Toxicol. Appl. Pharmacol. 164, 149-160.
53. Zhang, H., Zhang, Z., van der Lee, T., Chen, W.Q., Xu, J., Xu, J.S., Yang, L., Yu, D., Waalwijk, C. and Feng, J. (2010) Population genetic analyses of Fusarium asiaticum populations from barley suggest a recent shift favoring 3ADON producers in southern China. Phytopathology, 100, 328-336.