Characterization of genetic and biochemical mechanisms of fludioxonil and pyrimethanil resistance in field isolates of Penicillium digitatum

Phytopathology

Volumn 98, Issue 2, 2008, Pages 205-214

  Kanetis, L ^a   Forster H ^b   Jones, C A ^a   Borkovich, K A ^a   Adaskaveg, J E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Citrus green mold; Fungicide resistance

Indexed keywords

1,3 DIOXOLANE DERIVATIVE; FLUDIOXONIL; FUNGAL PROTEIN; PYRIMETHANIL; PYRIMIDINE DERIVATIVE; PYRROLE DERIVATIVE;

AMINO ACID SEQUENCE; ANTIFUNGAL RESISTANCE; ARTICLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PENICILLIUM; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; DIOXOLES; DRUG RESISTANCE, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; MOLECULAR SEQUENCE DATA; PENICILLIUM; PYRIMIDINES; PYRROLES; SEQUENCE HOMOLOGY, AMINO ACID;

BOTRYOTINIA FUCKELIANA; CITRUS; FUNGI; PENICILLIUM DIGITATUM;

EID: 39449133051     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-98-2-0205     Document Type: Article

References (52)

1. Atlas, R. M. 2004. Handbook of Microbiological Media. 3rd ed. L. C. Parks, ed. CRC Press, Boca Raton, FL.
2. Avenot, H., Simoneau, P., Iacomi-Vasilescu, B., and Betaille-Simoneau, N. 2005. Characterization of mutations in the two-component histidine kinase gene AbNIK1 from Alternaria brassicicola that confer high dicarboximide and phenylpyrrole resistance. Curr. Genet. 47:234-243.
3. Banno, S., Noguchi, R., Yamashita, K., Fukumori, F., Kimura, M., Yamaguchi, I., and Fugimura, M. 2007. Roles of putative His-to-Asp signaling modules HPT-1 and RRG-2, on viability and sensitivity to osmotic stresses in Neurospora crassa. Curr. Genet. 51:197-208.
4. Bus, V. G., Bongers, A. J., and Risse, L. A. 1991. Occurrence of Penicillium digitatum and P. italicum resistant to benomyl, thiabendazole, and imazalil on citrus from different geographic origins. Plant Dis. 75:1098-1100.
5. Catlett, N. L., Yoder, O. C., and Turgeon, B. G. 2003. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot. Cell 2:1151-1161.
6. Cui, W., Beever, R. E., Parkes, S. L., Weeds, P. L., and Templeton, M. D. 2002. An osmosensing histidine kinase mediates dicarboximide resistance in Botryotinia fuckeliana (Botrytis cinerea). Fungal Genet. Biol. 36:187-198.
7. Daniels, A., and Lucas, J. A. 1995. Mode of action of the anilinopyrimidine fungicide pyrimethanil. 1. In vivo activity against Botrytis fabae on broad bean (Vicia faba) leaves. Pestic. Sci. 45:33-41.
8. Dry, I. B., Yuan, K. H., and Hutton, D. G. 2004. Dicarboximide resistance in field isolates of Alternaria alternata is mediated by a mutation in a two-component hisitidine kinase gene. Fungal Genet. Biol. 41:102-108.
9. Eckert, J. W., and Eaks, I. L. 1989. Postharvest Disorders and Diseases of Citrus Fruit. Pages 179-260 in: The Citrus Industry, Volume V - Crop Protection, Postharvest Technology, and Early History of Citrus Research in California. W. Reuther, E. C. Calavan, and G. E. Carman, eds. University of California, Division of Agricultural and Natural Resources, Oakland, CA.
10. Errampalli, D. 2003. Effect of fludioxonil on germination and growth of Penicillium expansum and decay in apple cvs. Empire and Gala. Crop Prot. 23:822-827.
11. Förster, H., Driever, G. F., Thompson, D. C., and Adaskaveg, J. E. 2007. Postharvest decay management for stone fruit crops in California using the "reduced-risk" fungicides fludioxonil and fenhexamid. Plant Dis. 91:209-215.
12. Förster, H., Kanetis, L., and Adaskaveg, J. E. 2004. Spiral gradient dilution, a rapid method for determining growth responses and 50% effective concentration values in fungus-fungicide interactions. Phytopathology 94:163-170.
13. Fritz, R., Lanen, C., Chapeland-Leclerc, F., and Leroux, P. 2003. Effect of the anilinopyrimidine fungicide pyrimethanil on the cystathionine β-lyase of Botrytis cinerea. Pestic. Biochem. Phys. 77:54-65.
14. Fujimura, M., Ochiai, N., Ichiishi, A., Usami, R., Horikoshi, K., and Yamaguchi, I. 2000. Sensitivity to phenypyrrole fungicides and abnormal glycerol accumulation in os and cut mutant strains of Neurospora crassa. J. Pestic. Sci. 25:31-36.
15. Fujimura, M., Ochiai, N., Ichiishi, A., Usami, R., Horikoshi, K., and Yamaguchi, I. 2000. Fungicide sensitivity and osmotic stress sensitivity in os mutants of Neurospora crassa. Pestic. Biochem. Phys. 67:125-133.
16. Furukawa, K., Katsuno, Y., Urao, T., Yabe, T., Yamada-Okabe, T., Yamada-Okabe, H., Yamagata, Y., Abe, K., and Nakajima, T. 2002. Isolation and functional analysis of a gene, tcsB, encoding a transmembrane hybrid-type histidine kinase from Aspergillus nidulans. Appl. Environ. Microbiol. 68:5304-5310.
17. Gehmann, K., Nyfeler, R., Leadbeater, A. J., Nevill, D., and Sozzi, D. 1990. CGA 173506: A new phenylpyrrole fungicide for broad-spectrum disease control. Brighton Crop Prot. Conf. Pests Dis. 2:399-406.
18. Griffin, D. H. 1994. Fungal Physiology. 2nd ed. Wiley-Liss, Inc., New York, NY.
19. Hilber, U. W., and Hilber-Bodmer, M. 1996. Genetic basis and monitoring of resistance of Botryotinia fuckeliana to anilinopyrimidines. Plant Dis. 82:496-500.
20. Hilber, U. W., and Schüepp, H. 1996. A reliable method for testing the sensitivity of Botryotinia fuckeliana to anilinopyrimidines in vitro. Pestic. Sci. 47:241-247.
21. Holmes, G. J., and Eckert, J. W. 1999. Sensitivity of Penicillium digitatum and P. italicum to postharvest citrus fungicides in California. Phytopathology 89:716-721.
22. Iacomi-Vasilescu, B., Avenot, H., Betaile-Simoneau, N., Laurent, E., Guenard, M., and Simoneau, P. 2004. In vitro sensitivity of Alternaria species pathogenic to crucifers and identification of Alternaria brassicicola field isolates highly resistant to both dicarboximides and phenylpyrroles. Crop Prot. 23:481-488.
23. Irmler, S., Rogniaux, H., Hess, D., and Pillonel, C. 2006. Induction of OS-2 phosphorylation in Neurospora crassa by treatment with phenylpyrrole fungicides and osmotic stress. Pestic. Biochem. Phys. 84:25-37.
24. Jespers, A. B. K., and de Waard, M. A. 1995. Effect of fenpiclonil on phosphorylation of glucose in Fusarium sulphureum. Pestic. Sci. 44:167-175.
25. Jones, C. A., Greer-Phillips, S. E., and Borkovich, K. A. 2007. The response regulator RRG-1 functions upstream of a MAPK pathway impacting asexual development, female fertility, osmotic stress and fungicide resistance in Neurospora crassa. Mol. Biol. Cell 18:2123-2136.
26. Judelson, H. S. 1996. Genetic and physical variability at the mating type locus of the oomycete, Phytophthora infestans. Genetics 144:1005-1013.
27. Kanetis, L., and Adaskaveg, J. E. 2005. Resistance potential of azoxystrobin, fludioxonil, and pyrimethanil, to the citrus postharvest pathogen Penicillium digitatum. (Abstr.) Phytopathology 95(suppl.):S51.
28. Kanetis, L., Förster, H., and Adaskaveg, J. E. 2006. Fludioxonil-resistant isolates of Penicillium digitatum show diverse fitness and no relationship to osmotic stress regulation. (Abstr.) Phytopathology 96(suppl.):S58.
29. Kanetis, L., Förster, H., and Adaskaveg, J. E. 2007. Comparative efficacy of the new postharvest fungicides azoxystrobin, fludioxonil, and pyrimethanil for managing citrus green mold caused by Penicillium digitatum. Plant Dis. 91:1502-1511.
30. Kanetis, L., Förster, H., and Adaskaveg, J. E. 2007. Baseline sensitivities for new postharvest fungicides against Penicillium spp. on citrus and multiple resistance evaluations in P. digitatum. Plant Dis. (In Press.)
31. Kinay, P., Mansour, M. F., Mlikota-Gabler, F., Margosan, D. A., and Smilanick, J. L. 2007. Characterization of fungicide-resistant isolates of Penicillium digitatum collected in California. Crop Prot. 26:647-656.
32. Kojima, K., Takano, Y., Yoshimi, A., Tanaka, C., Kikuchi, T., and Okuno, T. 2004. Fungicide activity through activation of a fungal signaling pathway. Mol. Microbiol. 53:1785-1796.
33. Krystofova, S., and Borkovich, K. A. 2005. The heterotrimeric G-protein subunits GNG-1 and GNB-1 form a Gβγ dimer required for normal female fertility, asexual development, and Gα protein levels in Neurospora crassa. Eukaryot. Cell 4:365-378.
34. Latorre, B. A., Spadaro, I., and Rioja, M. E. 2002. Occurrence of resistant isolates of Botrytis cinerea to anilinopyrimidine fungicides in table grapes in Chile. Crop Prot. 21:957-961.
35. Leroux, P., Fritz, R., Debieu, D., Albertini, C., Lanen, C., Bach, J., Gredt, M., and Chapeland, F. 2002. Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag. Sci. 58:876-888.
36. Leroux, P., and Gredt, M. 1996. In vitro methods for monitoring pyrimethanil resistance of Botrytis cinerea in grapevine. EPPO Bull. 26:186-188.
37. Ma, Z., Luo, Y., and Michailides, T. 2006. Molecular characterization of the two-component histidine kinase gene from Monilinia fructicola. Pest Manag. Sci. 62:991-998.
38. Masner, P., Muster, P., and Schmid, J. 1994. Possible methionine biosynthesis inhibition by pyrimidinamine fungicides. Pestic. Sci. 42:163-166.
39. Milling, R. J., and Richardson, C. J. 1995. Mode of action of the aniline-pyrimidine fungicide pyrimethanil. Effects on enzyme secretion in Botrytis cinerea. Pestic. Sci. 45:43-48.
40. Miura, I., Kamakura, T., Maeno, S., Hayashi, S., and Yamaguchi, I. 1994. Inhibition enzyme secretion in plant pathogens by mepanipyrim, a novel fungicide. Pestic. Biochem. Phys. 48:222-228.
41. Motoyama, T., Ohira, T., Kadokura, K., Ichiishi, A., Fujimura, M., Yamaguchi, I., and Kudo, T. 2005. An Os-1 family histidine kinase from a filamentous fungus confers fungicide-resistance to yeast. Curr. Genet. 47:298-306.
42. Ochiai, N., Fujimura, M., Motoyama, T., Ichiishi, A., Usami, R., Horikoshi, K., and Yamaguchi, I. 2001. Characterization of mutations in the two-component histidine kinase gene that confer fludioxonil resistance and osmotic sensitivity in the os-1 mutants of Neurospora crassa. Pest Manag. Sci. 57:437-442.
43. Okada, A., Banno, S., Ichiishi, A., Kimura, M., Yamaguchi, I., and Fujimura, M. 2005. Pyrrolnitrin interferes with osmotic signal transduction in Neurospora crassa. J. Pestic. Sci. 30:378-383.
44. Orth, A. B., Rzhetskaya, M., Pell, E. J., and Tien, M. 1995. A serine (threonine) protein kinase confers fungicide resistance in the phytopathogenic fungus Ustilago maydis. Appl. Environ. Microbiol. 61:2341-2345.
45. Oshima, M., Fujimura, M., Banno, S., Hashimoto, C., Motoyama, T., Ichiishi, A., and Yamaguchi, I. 2002. A point mutation of the two-component histidine kinase BcOS-1 gene confers dicarboximide resistance in field isolates of Botrytis cinerea. Phytopathology 92:75-80.
46. Pillonel, C., and Meyer, T. 1997. Effect of phenylpyrroles on glycerol accumulation and protein kinase activity of Neurospora crassa. Pestic. Sci. 49:229-236.
47. Rosslenbloich, H. J., and Stuebler, D. 2000. Botrytis cinerea - History of chemical control and novel fungicides for its management. Crop Prot. 19:557-561.
48. Steel, C. C. 1996. Catalase activity and sensitivity to the fungicides, iprodione and fludioxonil in Botrytis cinerea. Lett. Appl. Microbiol. 22:335-338.
49. Vignutelli, A., Hilber-Bodmer, M., and Hilber, U. W. 2002. Genetic analysis of resistance to the phenylpyrrole fludioxonil and the dicarboximide vinclozolin in Botryotinia fuckeliana. Mycol. Res. 106:329-335.
50. Vogel, H. J. 1964. Distribution of lysine pathways among fungi: Evolutionary implications. Am. Nat. 98:435-446.
51. Yoshimi, A., Kojima, K., Takano, Y., and Tanaka, C. 2005. Type III histidine kinase is a positive regulator of Hog1-type mitogen-activated protein kinase in filamentous fungi. Eukaryot. Cell 4:1820-1828.
52. Zhang, Y., Lamm, R., Pillonel, C., Lam, S., and Xu, J. R. 2002. Osmoregulation and fungicide resistance: The Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl. Environ. Microbiol. 68:532-538.