Characterization of cytochrome b from European field isolates of Cercospora beticola with quinone outside inhibitor resistance

European Journal of Plant Pathology

Volumn 134, Issue 3, 2012, Pages 475-488

  Birla, Keshav ^a   Rivera Varas, Viviana ^a   Secor, Gary A ^a   Khan, Mohamed F R ^a,b   Bolton, Melvin D ^a,c  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Cercospora leaf spot (CLS); G143A; MAMA; Strobilurin; Sugar beet

Indexed keywords

AMINO ACID; CYTOCHROME; DISEASE CONTROL; ENZYME ACTIVITY; FUNGAL DISEASE; FUNGICIDE; GERMINATION; HOMOLOGY; INHIBITOR; MOLECULAR ANALYSIS; MONITORING; MUTATION; PESTICIDE RESISTANCE; RESISTANCE MANAGEMENT; SENSITIVITY ANALYSIS; SPORE; SUGAR BEET;

FRANCE; ITALY;

BETA VULGARIS SUBSP. VULGARIS; CERCOSPORA; CERCOSPORA BETICOLA;

EID: 84867138934     PISSN: 09291873     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10658-012-0029-y     Document Type: Article

References (44)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
2. Amand, O., Calay, F., Coquillart, L., Legat, T., Bodson, B., Moreau, J. M., & Maraite, H. (2003). First detection of resistance to QoI fungicides in Mycosphaerella graminicola on winter wheat in Belgium. Communications in Agricultural and Applied Biological Sciences, 68, 519.
3. Banno, S., Yamashita, K., Fukumori, F., Okada, K., Uekusa, H., Takagaki, M., Kimura, M., & Fujimura, M. (2009). Characterization of QoI resistance in Botrytis cinerea and identification of two types of mitochondrial cytochrome b gene. Plant Pathology, 58, 120-129.
4. Bartlett, D. W., Clough, J. M., Godwin, J. R., Hall, A. A., Hamer, M., & Parr-Dobrzanski, B. (2002). The strobilurin fungicides. Pest Management Science, 58, 649-662.
5. Bolton, M. D., Kolmer, J. A., & Garvin, D. F. (2008). Wheat leaf rust caused by Puccinia triticina. Molecular Plant Pathology, 9, 563-575.
6. Bolton, M. D., Birla, K., Rivera-Varas, V., Rudolph, K., & Secor, G. A. (2012a). Characterization of CbCyp51 from field isolates of Cercospora beticola. Phytopathology, 102, 298-305.
7. Bolton, M. D., Secor, G. A., Rivera, V., Weiland, J. J., Rudolph, K., Birla, K., Rengifo, J., & Campbell, L. G. (2012b). Evaluation of the potential for sexual reproduction in field populations of Cercospora beticola from USA. Fungal Biology, 116, 511-521.
8. Cha, R. S., Zarbl, H., Keohavong, P., & Thilly, W. G. (1992). Mismatch amplification mutation assay (MAMA): application to the cH-ras gene. Genome Research, 2, 14-20.
9. Chin, K. M., Chavaillaz, D., Kaesbohrer, M., Staub, T., & Felsenstein, F. G. (2001). Characterizing resistance risk of Erysiphe graminis f. sp. tritici to strobilurins. Crop Protection, 20, 87-96.
10. Daub, M. E., & Ehrenshaft, M. (2000). The photoactivated Cercospora toxin cercosporin: contributions to plant disease and fundamental biology. Annual Reviews in Phytopathology, 38, 461-490.
11. Fisher, N., & Meunier, B. (2008). Molecular basis of resistance to cytochrome bc1 inhibitors. FEMS Yeast Research, 8, 183-192.
12. Fontaine, S., Remuson, F., Fraissinet-Tachet, L., Micoud, A., Marmeisse, R., & Melayah, D. (2009). Monitoring of Venturia inaequalis harbouring the QoI resistance G143A mutation in French orchards as revealed by PCR assays. Pest Management Science, 65, 74-81.
13. Fraaije, B. A., Butters, J. A., Coelho, J. M., Jones, D. R., & Hollomon, D. W. (2002). Following the dynamics of strobilurin resistance in Blumeria graminis f. sp. tritici using quantitative allele-specific real-time PCR measurements with the fluorescent dye SYBR Green I. Plant Pathology, 51, 45-54.
14. FRAC. (2011). FRAC list of plant pathogenic organisms resistant to disease control agents.
15. Gisi, U., Sierotzki, H., Cook, A., & McCaffery, A. (2002). Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Management Science, 58, 859-867.
16. Grasso, V., Palermo, S., Sierotzki, H., Garibaldi, A., & Gisi, U. (2006). Cytochrome b gene structure and consequences for resistance to Qo inhibitor fungicides in plant pathogens. Pest Management Science, 62, 465-472.
17. Gressel, J. (2011). Low pesticide rates may hasten the evolution of resistance by increasing mutation frequencies. Pest Management Science, 67, 253-257.
18. Groenewald, M., Groenewald, J. Z., Linde, C. C., & Crous, P. W. (2007). Development of polymorphic microsatellite and single nucleotide polymorphism markers for Cercospora beticola (Mycosphaerellaceae). Molecular Ecology Notes, 7, 890-892.
19. Groenewald, M., Linde, C. C., Groenewald, J. Z., & Crous, P. W. (2008). Indirect evidence for sexual reproduction in Cercospora beticola populations from sugar beet. Plant Pathology, 57, 25-32.
20. Hily, J.-M., Singer, S. D., Villani, S. M., & Cox, K. D. (2011). Characterization of the cytochrome b (cyt b) gene from Monilinia species causing brown rot of stone and pome fruit and its significance in the development of QoI resistance. Pest Management Science, 67, 385-396.
21. Kaiser, U., Kluth, C., & Märländer, B. (2010). Variety-specific epidemiology of Cercospora beticola Sacc. and consequences for threshold-based timing of fungicide application in sugar beet. Journal of Phytopathology, 158, 296-306.
22. Karaoglanidis, G. S., & Ioannidis, P. M. (2010). Fungicide resistance of Cercospora beticola in Europe. In R. T. Lartey, J. J. Weiland, L. Panella, P. W. Crous, & C. E. Windels (Eds.), Cercospora leaf spot of sugar beet and related species. St. Paul: The American Phytopathological Society.
23. Khan, J., Qi, A., & Khan, M. F. R. (2009). Fluctuations in number of Cercospora beticola conidia in relationship to environment and disease severity in sugar beet. Phytopathology, 99, 796-801.
24. Kim, Y. S., Dixon, E. W., Vincelli, P., & Farman, M. L. (2003). Field resistance to strobilurin (QoI) fungicides in Pyricularia grisea caused by mutations in the mitochondrial cytochrome b gene. Phytopathology, 93, 891-900.
25. Lesniak, K. E., Proffer, T. J., Beckerman, J. L., & Sundin, G. W. (2011). Occurrence of QoI resistance and detection of the G143A mutation in Michigan populations of Venturia inaequalis. Plant Disease, 95, 927-934.
26. Luo, C. X., Hu, M. J., Jin, X., Yin, L. F., Bryson, P. K., & Schnabel, G. (2010). An intron in the cytochrome b gene of Monilinia fructicola mitigates the risk of resistance development to QoI fungicides. Pest Management Science, 66, 1308-1315.
27. Malandrakis, A., Markoglou, A., Nikou, D., Vontas, J., & Ziogas, B. (2006). Biological and molecular characterization of laboratory mutants of Cercospora beticola resistant to Qo inhibitors. European Journal of Plant Pathology, 116, 155-166.
28. Malandrakis, A. A., Markoglou, A. N., Nikou, D. C., Vontas, J. G., & Ziogas, B. N. (2011). Molecular diagnostic for detecting the cytochrome b G143S - QoI resistance mutation in Cercospora beticola. Pesticide Biochemistry and Physiology, 100, 87-92.
29. McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349-379.
30. Milgroom, M. G. (1996). Recombination and the multilocus structure of fungal populations. Annual Review of Phytopathology, 34, 457-477.
31. Moretti, M., Karaoglanidis, G., Saracchi, M., Fontana, A., & Farina, G. (2006). Analysis of genotypic diversity in Cercospora beticola Sacc. field isolates. Annals of Microbiology, 56, 215-221.
32. Pasche, J. S., Piche, L. M., & Gudmestad, N. C. (2005). Effect of the F129L mutation in Alternaria solani on fungicides affecting mitochondrial respiration. Plant Disease, 89, 269-278.
33. Roohparvar, R., Mehrabi, R., van Nistelrooy, J. G., Zwiers, L. H., & De Waard, M. A. (2008). The drug transporter MgMfs1 can modulate sensitivity of field strains of the fungal wheat pathogen Mycosphaerella graminicola to the strobilurin fungicide trifloxystrobin. Pest Management Science, 64, 685-693.
34. Secor, G. A., & Rivera, V. V. (2012). Fungicide resistance assays for fungal plant pathogens. In M. D. Bolton & B. P. H. J. Thomma (Eds.), Plant fungal pathogens: Methods and protocols (pp. 385-392). New York: Humana Press.
35. Secor, G. A., Rivera, V. V., Khan, M. F. R., & Gudmestad, N. C. (2010). Monitoring fungicide sensitivity of Cercospora beticola of sugar beet for disease management decisions. Plant Disease, 94, 1272-1282.
36. Siah, A., Deweer, C., Morand, E., Reignault, P., & Halama, P. (2010). Azoxystrobin resistance of French Mycosphaerella graminicola strains assessed by four in vitro bioassays and by screening of G143A substitution. Crop Protection, 29, 737-743.
37. Sierotzki, H., Wullschleger, J., & Gisi, U. (2000). Point mutation in cytochrome b gene conferring resistance to strobilurin fungicides in Erysiphe graminis f. sp. tritici field solates. Pesticide Biochemistry and Physiology, 68, 107-112.
38. Sierotzki, H., Frey, R., Wullschleger, J., Palermo, S., Karlin, S., Godwin, J., & Gisi, U. (2007). Cytochrome b gene sequence and structure of Pyrenophora teres and P. tritici-repentis and implications for QoI resistance. Pest Management Science, 63, 225-233.
39. Steinkamp, M. P., Martin, S. S., Hoefert, L. L., & Ruppel, E. G. (1979). Ultrastructure of lesions produced by Cercospora beticola in leaves of Beta vulgaris. Physiol. Plant Pathol, 15, 13-26.
40. Stewart, C., & Via, L. E. (1993). A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. BioTechniques, 14, 748-749.
41. Torriani, S. F. F., Brunner, P. C., McDonald, B. A., & Sierotzki, H. (2009). QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Management Science, 65, 155-162.
42. USDA Foreign Agricultural Service. (2011). EU-27 Sugar Annual. GAIN Report Number: E60021.
43. van den Bosch, F., Paveley, N., Shaw, M., Hobbelen, P., & Oliver, R. (2011). The dose rate debate: does the risk of fungicide resistance increase or decrease with dose? Plant Pathology, 60, 597-606.
44. Zheng, D., Olaya, G., & Köller, W. (2000). Characterization of laboratory mutants of Venturia inaequalis resistant to the strobilurin-related fungicide kresoxim-methyl. Current Genetics, 38, 148-155.