Adaptation of Fusarium graminearum to tebuconazole yielded descendants diverging for levels of fitness, fungicide resistance, virulence, and mycotoxin production

Phytopathology

Volumn 100, Issue 5, 2010, Pages 444-453

  Becher, Rayko ^a   Hettwer, Ursula ^b   Karlovsky, Petr ^b   Deising, Holger B ^a   Wirsel, Stefan G R ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

DMIs; Fenpropimorph; Gibberella zeae; Prochloraz; Prothioconazole; Spiroxamine; Trichothecene; Zearalenone

Indexed keywords

FUNGICIDE; MYCOTOXIN; TEBUCONAZOLE; TRIAZOLE DERIVATIVE;

ANTIFUNGAL RESISTANCE; ARTICLE; BIOSYNTHESIS; DRUG EFFECT; FUSARIUM; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; VIRULENCE; WHEAT;

DRUG RESISTANCE, FUNGAL; FUNGICIDES, INDUSTRIAL; FUSARIUM; MYCOTOXINS; PLANT DISEASES; TRIAZOLES; TRITICUM; VIRULENCE;

FUSARIUM; GIBBERELLA ZEAE;

EID: 77951942995     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-100-5-0444     Document Type: Article

References (53)

1. Adejumo, T. O., Hettwer, U., and Karlovsky, P. 2007. Survey of maize from south-western Nigeria for zearalenone, alpha- and beta-zearalenols, fumonisin B-1 and enniatins produced by Fusarium species. Food Addit. Contam. 24:993-1000. (Pubitemid 47263918)
2. Akallal, R., Debieu, D., Lanen, C., Daboussi, M. J., Fritz, R., Malosse, C., Bach, J., and Leroux, P. 1998. Inheritance and mechanisms of resistance to tebuconazole, a sterol C14-demethylation inhibitor, in Nectria haematococca. Pestic. Biochem. Physiol. 60:147-166. (Pubitemid 28362212)
3. Bai, G. H., Chen, L. F., and Shaner, G. 2003. Breeding for resistance to Fusarium head blight of wheat in China. Pages 296-317 in: Fusarium Head Blight of Wheat and Barley. K. J. Leonard and W. R. Bushnell, eds. The American Phytopathological Society, St. Paul, MN. (Pubitemid 36599809)
4. Bai, G. H., and Shaner, G. 1996. Variation in Fusarium graminearum and cultivar resistance to wheat scab. Plant Dis. 80:975-979. (Pubitemid 126754685)
5. Barug, D., and Kerkenaar, A. 1984. Resistance in mutagen-induced mutants of Ustilago maydis to fungicides which inhibit ergosterol biosynthesis. Pestic. Sci. 15:78-84.
6. Brandfass, C., and Karlovsky, P. 2008. Upscaled CTAB-based DNA extraction and real-time PCR assays for Fusarium culmorum and F. graminearum DNA in plant material with reduced sampling error. Int. J. Mol. Sci. 9:2306-2321.
7. Brent, K. J., and Hollomon, D. W. 2007. Fungicide resistance: The assessment of risk. FRAC Monogr. No. 2, 2nd ed. Fungicide Resistance Action Committee, Brussels.
8. Buchenauer, H. 1987. Mechanism of action of triazolyl fungicides and related compounds. Pages 205-232 in: Modern Selective Fungicides. H. Lyr, ed. Gustav-Fischer-Verlag, Jena, Germany.
9. Chen, Y., and Zhou, M. G. 2009. Sexual recombination of carbendazim resistance in Fusarium graminearum under field conditions. Pest. Manage. Sci. 65:398-403.
10. Cowen, L. E. 2001. Predicting the emergence of resistance to antifungal drugs. FEMS Microbiol. Lett. 204:1-7.
11. Cowen, L. E., Anderson, J. B., and Kohn, L. M. 2002. Evolution of drug resistance in Candida albicans. Annu. Rev. Microbiol. 56:139-165. (Pubitemid 35217451)
12. Cowen, L. E., Sanglard, D., Calabrese, D., Sirjusingh, C., Anderson, J. B., and Kohn, L. M. 2000. Evolution of drug resistance in experimental populations of Candida albicans. J. Bacteriol. 182:1515-1522. (Pubitemid 30121114)
13. Debieu, D., Gall, C., Gredt, M., Bach, J., Malosse, C., and Leroux, P. 1992. Ergosterol biosynthesis and its inhibition by fenpropimorph in Fusarium species. Phytochemistry 31:1223-1233.
14. Desjardins, A. E. 2006. Fusarium Mycotoxins: Chemistry, Genetics, and Biology. The American Phytopathological Society, St. Paul, MN.
15. De Waard, M. A., Andrade, A. C., Hayashi, K., Schoonbeek, H. J., Stergiopoulos, I., and Zwiers, L. H. 2006. Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manage. Sci. 62:195-207.
16. De Waard, M. A., Georgopoulos, S. G., Hollomon, D. W., Ishii, H., Leroux, P., Ragsdale, N. N., and Schwinn, F. J. 1993. Chemical control of plant diseases - problems and prospects. Annu. Rev. Phytopathol. 31:403-421. (Pubitemid 2001605)
17. De Waard, M. A., Groeneweg, H., and Van Nistelrooy, J. G. M. 1982. Laboratory resistance to fungicides which inhibit ergosterol biosynthesis in Penicillium italicum. Neth. J. Plant Pathol. 88:99-112.
18. De Waard, M. A., and Van Nistelrooy, J. G. M. 1988. Accumulation of SBI fungicides in wild-type and fenarimol-resistant isolates of Penicillium italicum. Pestic. Sci. 22:371-382.
19. De Waard, M. A., and Van Nistelrooy, J. G. M. 1990. Stepwise development of laboratory resistance to DMI-fungicides in Penicillium italicum. Neth. J. Plant Pathol. 96:321-329.
20. Dill-Macky, R., and Jones, R. K. 2000. The effect of previous crop residues and tillage on Fusarium head blight of wheat. Plant Dis. 84:71-76. (Pubitemid 30023503)
21. FAO. 2004. Worldwide regulations for mycotoxins in food and feed in 2003. FAO Food and Nutrition Papers No. 81. Food and Agriculture Organization of the United Nations, Rome.
22. Godet, F., and Limpert, E. 1998. Recent evolution of multiple resistance of Blumeria (Erysiphe) graminis f. sp. tritici to selected DMI and morpholine fungicides in France. Pestic. Sci. 54:244-252. (Pubitemid 28504255)
23. Goswami, R. S., and Kistler, H. C. 2005. Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology 95:1397-1404.
24. Hamamoto, H., Hasegawa, K., Nakaune, R., Lee, Y. J., Makizumi, Y., Akutsu, K., and Hibi, T. 2000. Tandem repeat of a transcriptional enhancer upstream of the sterol 14 alpha-demethylase gene (CYP51) in Penicillium digitatum. Appl. Environ. Microbiol. 66:3421-3426. (Pubitemid 30624585)
25. Joseph-Horne, T., Hollomon, D., Manning, N., and Kelly, S. L. 1996. Investigation of the sterol composition and azole resistance in field isolates of Septoria tritici. Appl. Environ. Microbiol. 62:184-190. (Pubitemid 26013389)
26. Joseph-Horne, T., Manning, N. J., Hollomon, D., and Kelly, S. L. 1995. Defective sterol Δ5(6) desaturase as a cause of azole resistance in Ustilago maydis. FEMS Microbiol. Lett. 127:29-34.
27. Julian, A. M., Hardy, J. E., and Lucas, J. A. 1994. The induction and characterization of isolates of Pseudocercosporella herpotrichoides with altered sensitivity to the fungicide prochloraz. Pestic. Sci. 41:121-128.
28. Kalamarakis, A. E., De Waard, M. A., Ziogas, B. N., and Georgopoulos, S. G. 1991. Resistance to fenarimol in Nectria haematococca var. cucurbitae. Pestic. Biochem. Physiol. 40:212-220.
29. Klix, M. B., Verreet, J. A., and Beyer, M. 2007. Comparison of the declining triazole sensitivity of Gibberella zeae and increased sensitivity achieved by advances in triazole fungicide development. Crop Prot. 26:683-690. (Pubitemid 46136686)
30. Kuck, K. H., Scheinpflug, H., and Pontzen, R. 1995. DMI fungicides. 205-258 in: Modern Selective Fungicides. H. Lyr, ed. Gustav-Fischer-Verlag, Jena, Germany.
31. Leroux, P., Albertini, C., Gautier, A., Gredt, M., and Walker, A. S. 2007. Mutations in the CYP51 gene correlated with changes in sensitivity to sterol 14 alpha-demethylation inhibitors in field isolates of Mycosphaerella graminicola. Pest Manage. Sci. 63:688-698. (Pubitemid 47025963)
32. Lysoe, E., Klemsdal, S. S., Bone, K. R., Frandsen, R. J. N., Johansen, T., Thrane, U., and Giese, H. 2006. The PKS4 gene of Fusarium graminearum is essential for zearalenone production. Appl. Environ. Microbiol. 72:3924-3932. (Pubitemid 43894853)
33. Madden, L. V., Knoke, J. K., and Louie, R. 1982. Considerations for the use of multiple comparison procedures in phytopathological investigations. Phytopathology 72:1015-1017.
34. Maier, F. J., Miedaner, T., Hadeler, B., Felk, A., Salomon, S., Lemmens, M., Kassner, H., and Schafer, 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. (Pubitemid 44607167)
35. Mavroeidi, V. I., and Shaw, M. W. 2005. Sensitivity distributions and cross-resistance patterns of Mycosphaerella graminicola to fluquin-conazole, prochloraz and azoxystrobin over a period of 9 years. Crop Prot. 24:259-266.
36. Mesterházy, Á. 2003. Control of Fusarium head blight of wheat by fungicides. Pages 363-380 in: Fusarium Head Blight of Wheat and Barley. K. J. Leonard and W. R. Bushnell, eds. The American Phytopathological Society, St. Paul, MN.
37. Mukhopadhyay, K., Prasad, T., Saini, P., Pucadyil, T. J., Chattopadhyay, A., and Prasad, R. 2004. Membrane sphingolipid-ergosterol interactions are important determinants of multidrug resistance in Candida albicans. Antimicrob. Agents Chemother. 48:1778-1787. (Pubitemid 38544389)
38. Nakaune, R., Adachi, K., Nawata, O., Tomiyama, M., Akutsu, K., and Hibi, T. 1998. A novel ATP-binding cassette transporter involved in multidrug resistance in the phytopathogenic fungus Penicillium digitatum. Appl. Environ. Microbiol. 64:3983-3988. (Pubitemid 28463003)
39. O'Donnell, K., Kistler, H. C., Tacke, B. K., and Casper, H. H. 2000. Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc. Natl. Acad. Sci. USA 97:7905-7910. (Pubitemid 30460746)
40. O'Donnell, K., Ward, T. J., Geiser, D. M., Kistler, H. C., and Aoki, T. 2004. Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet. Biol. 41:600-623. (Pubitemid 38581869)
41. Parry, D. W., Jenkinson, P., and McLeod, L. 1995. Fusarium ear blight (scab) in small grain cereals - a review. Plant Pathol. 44:207-238. (Pubitemid 26452727)
42. Reimann, S., and Deising, H. B. 2005. Inhibition of efflux transporter-mediated fungicide resistance in Pyrenophora tritici-repentis by a derivative of 4′-hydroxyflavone and enhancement of fungicide activity. Appl. Environ. Microbiol. 71:3269-3275. (Pubitemid 40807238)
43. Rotter, B. A., Prelusky, D. B., and Pestka, J. J. 1996. Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 48:1-34. (Pubitemid 26161162)
44. Schnabel, G., and Jones, A. L. 2001. The 14 alpha-demethylase (CYP51A1) gene is overexpressed in Venturia inaequalis strains resistant to myclobutanil. Phytopathology 91:102-110. (Pubitemid 32145010)
45. Schoustra, S. E., Debets, A. J. M., Slakhorst, M., and Hoekstra, R. F. 2006. Reducing the cost of resistance; experimental evolution in the filamentous fungus Aspergillus nidulans. J. Evol. Biol. 19:1115-1127. (Pubitemid 43918149)
46. Selmecki, A., Gerami-Nejad, M., Paulson, C., Forche, A., and Berman, J. 2008. An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol. Microbiol. 68:624-641. (Pubitemid 351490182)
47. Serfling, A., Wohlrab, J., and Deising, H. B. 2007. Treatment of a clinically relevant plant-pathogenic fungus with an agricultural azole causes cross-resistance to medical azoles and potentiates caspofungin efficacy. Antimicrob. Agents Chemother. 51:3672-3676. (Pubitemid 47519358)
48. Stehmann, C., and De Waard, M. A. 1996. Sensitivity of populations of Botrytis cinerea to triazoles, benomyl and vinclozolin. Eur. J. Plant Pathol. 102:171-180. (Pubitemid 27003931)
49. Wellmann, H., and Schauz, K. 1992. DMI-Resistance in Ustilago maydis. I. Characterization and genetic analysis of triadimefon-resistant laboratory mutants. Pestic. Biochem. Physiol. 43:171-181.
50. Wellmann, H., Schauz, K., and Tiemann, R. 1996. Resistance to sterol demethylation inhibitors in Ustilago maydis. III. Cross-resistance patterns and sterol analyses. Pestic. Sci. 48:239-246. (Pubitemid 27012257)
51. Wyand, R. A., and Brown, J. K. M. 2005. Sequence variation in the CYP51 gene of Blumeria graminis associated with resistance to sterol demethylase inhibiting fungicides. Fungal Genet. Biol. 42:726-735.
52. Yin, Y., Liu, X., Li, B., and Ma, Z. 2009. Characterization of sterol demethylation inhibitor-resistant isolates of Fusarium asiaticum and F. graminearum collected from wheat in China. Phytopathology 99:487-497.
53. Zinedine, A., Soriano, J. M., Molto, J. C., and Manes, J. 2007. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: An oestrogenic mycotoxin. Food Chem. Toxicol. 45:1-18. (Pubitemid 44792326)