Imazalil resistance linked to a unique insertion sequence in the PdCYP51 promoter region of Penicillium digitatum

Postharvest Biology and Technology

Volumn 44, Issue 1, 2007, Pages 9-18

  Ghosoph, Jennifer M ^a   Schmidt, Leigh S ^a   Margosan, Dennis A ^b   Smilanick, Joseph L ^b  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

14 Demethylase CYP51 gene; Demethylation inhibitors (DMIs); Fungicide resistance; Imazalil; Penicillium digitatum

Indexed keywords

CITRUS; PENICILLIUM DIGITATUM;

EID: 33847618261     PISSN: 09255214     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.postharvbio.2006.11.008     Document Type: Article

References (43)

1. Buchenauer H. Mode of action and selectivity of (systemic) fungicides which interfere with ergosterol biosynthesis in Ustilago avenae. Proceedings of 1977 British Crop Protection Conference-Pests and Diseases. British Crop Protection Council. Alton Hampshire, UK (1977) 699-711
2. Bus V.G., Bongers A.J., and Risse L.A. Occurrence of Penicillium digitatum and P. italicum resistant to benomyl, thiabendazole, and imazalil on citrus fruit from different geographic origins. Plant Dis. 75 (1991) 1098-1100
3. Chen D.H., and Ronald P.C. A rapid DNA minipreparation method suitable for AFLP and other PCR applications. Plant Mol. Biol. Rep. 17 (1999) 53-57
4. Dave B., Sales M., and Walia M. Resistance of different strains of Penicillium digitatum to imazalil treatment in California citrus packinghouses. Proc. FL. State Hortic. Soc. 102 (1989) 178-179
5. Delye C., Laigret F., and Corio-Costet M.-F. A mutation in the 14 alpha-demethylase gene of Uncinula necator that correlates with resistance to a sterol biosynthesis inhibitor. Appl. Environ. Microbiol. 63 (1997) 2966-2970
6. Delye C., Bousset L., and Corio-Costet M.-F. PCR cloning and detection of point mutations in the eburicol 14α-demethylase (CYP51) gene from Erysiphe graminis f. sp. hordei, a "recalcitrant" fungus. Curr. Genet. 34 (1998) 399-403
7. De Waard M.A. Resistance to fungicides which inhibit sterol 14α-demethylation, an historical perspective. In: Heaney S., Slawson D., Hollomon D.W., Smith M., Russels P.E., and Parry D.W. (Eds). Fungicide Resistance (1994), British Crop Protect. Council, Surrey, United Kingdom 3-10
8. De Waard M.A., and Van Nistelrooy J.G.M. An energy-dependent efflux mechanism for fenarimol in a wild type strain and fenarimol-resistant mutation of Aspergillus nidulans. Pesticide Biochem. Physiol. 13 (1980) 255-266
9. De Waard M.A., and Van Nistelrooy J.G.M. Induction of fenarimol-efflux activity in Aspergillus nidulans by fungicides inhibiting sterol biosynthesis. J. Gen. Microbiol. 126 (1981) 483-489
10. De Waard M.A., and Van Nistelrooy J.G.M. Differential accumulation of fenarimol by a wild type isolate and fenarimol-resistant isolates of Penicillium italicum. Neth. J. Plant Pathol. 90 (1984) 143-153
11. De Waard M.A., and Van Nistelrooy J.G.M. Inhibitors of energy-dependent efflux of fungicide fenarimol by Aspergillus nidulans. Exp. Mycol. 11 (1987) 1-10
12. Dupont J., Magnin S., Marti A., and Brousse M. Molecular tools for identification of Penicillium starter cultures used in the food industry. Int. J. Food Microbiol. 49 (1999) 109-118
13. Eckert J.W. Penicillium digitatum biotypes with reduced sensitivity to imazalil. Abstr. Phytopathology 77 (1987) 1728
14. Eckert J.W., and Wild B.L. Problems of fungicide resistance in Penicillium rot of citrus fruits. In: Georghiou G.P., and Saito T. (Eds). Pest Resistance to Pesticides (1983), Plenum Publishing Corp., New York, NY 525-556
15. Eckert J.W., Sievert J.R., and Ratnayake M. Reduction of imazalil effectiveness against citrus green mold in California packinghouses by resistant biotypes of Penicillium digitatum. Plant Dis. 78 (1994) 971-974
16. Geisen R., Cantor M.D., Hansen T.K., Holzapfel W.H., and Jakobsen M. Characterization of Penicillium roqueforti strains used as cheese starter cultures by RAPD typing. Int. J. Food Microbiol. 65 (2001) 183-191
17. Hamamoto H., Hasegawa K., Nakaune R., Jin Lee Y., Makizumi Y., Akutsu K., and Hibi T. Tandem repeat of a transcriptional enhancer upstream of the sterol 14α-demethylase (CYP51) in Penicillium digitatum. Appl. Environ. Microbiol. 66 (2000) 3421-3426
18. Hamamoto H., Haseqawa K., Nakaune R., Jin Lee Y., Akutsu K., and Hibi T. PCR-based detection of sterol demethylation inhibitor-resistant strains of Penicillium digitatum. Pest. Manage. Sci. 57 (2001) 839-843
19. Hamamoto H., Nawata O., Hasegawa K., Nakaune R., Jin Lee Y., Makizumi Y., Akutsu K., and Hibi T. The role of the ABC transporter gene PMR1 in demethylation inhibitor resistance in Penicillium digitatum. Pest. Biochem. Physiol. 70 (2001) 19-26
20. Harding Jr. P.R. R23979, a new imidazole derivative effective against postharvest decay of citrus by molds resistant to thiabendazole, benomyl, and 2-aminobutane. Plant Dis. Rep. 60 (1976) 643-646
21. Holloman D.W. Resistance to azole fungicides in the field. Biochem. Soc. Trans. 21 (1993) 1047-1051
22. Holmes G.J., and Eckert J.W. Relative fitness of imazalil-resistant and sensitive biotypes of Penicillium digitatum. Plant Dis. 79 (1995) 1068-1073
23. Holmes G.J., and Eckert J.W. Sensitivity of Penicillium digitatum and P. italicum to postharvest citrus fungicides in California. Phytopathology 89 (1999) 716-721
24. Ma Z., and Michailides T.J. Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Prot. 24 (2005) 853-863
25. Ma Z., Proffer T.J., Jacobs J.L., and Sundin G.W. Overexpression of the 14α-demethylase target gene (CYP51) mediates fungicide resistance in Blumeriella jaapii. Appl. Environ. Microbiol. 72 (2006) 2581-2585
26. Nakune R., Adachi K., Nawata O., Tomiyama M., Akutsu K., and Hibi T. A novel ATP-banding cassette transporter involved in multidrug resistance in the phytopathogenic fungi Penicillium digitatum. Appl. Environ. Microbiol. 64 (1998) 3983-3988
27. Nakune R., Hamamoto H., Imada K., Akutsu K., and Hibi T. A novel ABC transporter gene, PMR5, is involved in multidrug resistance in the phytophthogenic fungus Penicillium digitatum. Mol. Genet. Genomics 267 (2002) 179-185
28. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucl. Acids Res. 29 (2001) 2002-2007
29. Pianzzola M.J., Moscatelli M., and Vero S. Characterization of Penicillium isolates associated with blue mold on apple in Uruguay. Plant Dis. 88 (2004) 23-28
30. Rasmussen R. Quantification on the LightCycler. In: Meuer S., Wittwer C., and Nakagawara K. (Eds). Rapid Cycle Real-time PCR, Methods and Applications (2001), Springer Press, Heidelberg, Germany 21-34
31. Rebellato L.H., and Monteiro M.C. Report of an imazalil resistant strain of Penicillium digitatum in citrus in Uruguay. Proc. Int. Assoc. Citricult. 1 (1984) 588-590
32. In: Sambrook J., and Russell D.W. (Eds). Molecular Cloning: A Laboratory Manual. 3rd ed. (2001), Cold Spring Harbor Laboratory Press, New York, NY
33. Sanglard D., Kuchler K., Ischer F., Pagani J.L., Monod M., and Bille J. Mechanisms of resistance to azole antifungal agents in Candida albicans isolates from AIDS patients involve specific multidrug transporter. Antimicrob. Agents Chemother. 39 (1995) 2378-2386
34. Sanglard D., Ischer F., Koymans L., and Bille J. Amino acid substitutions in the cytochrome P0450 lanosterol 14α-demethylase (CPY51A1) from azole-resistant Candida albicans clinical isolates contribute to resistance to azole antifungal agents. Antimicrob. Agents Chemother. 42 (1998) 241-253
35. Schnabel G., and Jones A.L. The 14α-demethylase (CYP51A1) gene is overexpressed in Venturia inaequalis strains resistant to myclobutanil. Phytopathology 91 (2001) 102-110
36. Stehmann C., and De Waard M.A. Accumulation of tebuconazole by isolates of Botrytis cinerea differing in sensitivity to sterol demethylation inhibiting fungicides. Pectic. Sci. 45 (1995) 311-318
37. Van den Brink J.M., Van Nistelrooy J.G.M., De Waard M.A., Van den Hondel C.A., and Van Gorcom R.F. Increased resistance to 14 alpha-demethylase inhibitors (DMIs) in Aspergillus niger by coexpression of the Penicllium italicum eburicol 14 alpha-demethylase (cyp51) and the A. niger cytochrome P450 reductase (cprA) genes. J. Biotechnol. 49 (1996) 13-18
38. Vanden Bossche H., Marichal P., Gorrens J., Bellens D., Verhoeven H., Coene M.C., Lauwers W., and Janssen P.A. Interaction of azole derivatives with cytochrome P-450 isozymes in yeast, fungi, plants, and mammalian cells. Pestic. Sci. 21 (1987) 289-306
39. White T.C. Increased mRNA levels of Erg16, CDR, and MDR1 correlate with the increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob. Agents Chemother. 41 (1997) 1482-1487
40. Wild B.L. Differential sensitivity of citrus green mould isolates (Penicillium digitatum Sacc.) to the fungicide imazalil. N. Z. J. Crop Hortic. Sci. 22 (1994) 167-171
41. Wyand R.A., and Brown J.K.M. Sequence variation in the CYP51 gene of Blumeria graminis associated with resistance to sterol demethylase inhibiting fungicides. Fungal Genet. Biol. 42 (2005) 726-765
42. 14DM purified from Saccharomyces cerevisiae microsomes. Biochem. Pharmacol. 36 (1987) 229-235
43. 14DM) of yeast. Biochem. Soc. Trans. 19 (1991) 778-782