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Fungicide Resistance—Lessons for Herbicide Resistance Management?

Published online by Cambridge University Press:  12 June 2017

Tobin L. Peever
Affiliation:
Dep. Plant Pathol., Cornell Univ., Ithaca, NY 14853
Michael G. Milgroom
Affiliation:
Dep. Plant Pathol., Cornell Univ., Ithaca, NY 14853

Extract

Resistance to agricultural fungicides has increaséd dramatically in the past twenty years, following the introduction of systemic fungicides. Disease control failures associated with fungicide resistance have occurred with many classes of fungicides and in many genera of plant-pathogenic fungi. In some cases, resistance evolved extremely rapidly making the chemicals ineffective for disease control only a few years after they were introduced.

The rapid development of resistance to systemic fungicides has led to efforts to develop strategies to avoid or delay the evolution of fungicide resistance in plant pathogen populations. Despite a widespread interest in managing fungicide resistance, very few experimental studies have been performed to elucidate the important factors controlling resistance development. Most fungicide resistance studies have consisted of anecdotal field observations which have rarely been followed up with experimentation. In order to understand what factors affect the evolution of resistance, and to use this information to design effective resistance management strategies, more experimental studies are required.

Type
Symposium
Copyright
Copyright © 1995 by the Weed Science Society of America 

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References

Literature Cited

1. Bodmer, M., Hilber, U. W., and Köller, W. D. 1993. Fitness of Venturia inequalis strains with different sensitivities to DMI fungicides. Proc. 6th Int. Congr. Plant Pathol., Montreal, Canada. p. 56.Google Scholar
2. Bohnen, K., Pfiffner, A., Siegle, H., and Zobrist, P. 1986. Fenpropidin, a new systemic cereal mildew fungicide. Br. Crop Prot. Conf.—Pests and Dis. 1986. p. 2731.Google Scholar
3. Bolton, N.J.E. and Smith, J. M. 1988. Strategies to combat fungicide resistance in barley powdery mildew. Br. Crop Prot. Conf.—Pests and Dis. 1988. p. 367372.Google Scholar
4. Brent, K. J., Carter, G. A., Hollomon, D. W., Hunter, T., Locke, T., and Proven, M. 1989. Factors affecting buildup of fungicide resistance in powdery mildew in spring barley. Neth. J. Plant Pathol. 95 (Suppl. 1): 3141.Google Scholar
5. Buchenauer, H., Budde, K., Hellwald, K. H., Taube, E., and Kirchner, R., 1984. Decreased sensitivity of barley powdery mildew isolates to triazole and related fungicides. Br. Crop Prot. Conf.—Pests and Dis. 1984. p. 483488.Google Scholar
6. Butters, J. A., Clark, J., and Hollomon, D. W. 1984. Resistance to inhibitors of sterol biosynthesis in barley powdery mildew. Med. Fac. Landbouww. Rijksuniv. Gent 49:143151.Google Scholar
7. Chin, K. M. 1987. A simple model of selection for fungicide resistance in plant pathogen populations. Phytopathology 77:666669.Google Scholar
8. Clerjeau, M., Irhir, H., Moreau, C., Piganeau, B., Staub, T., and Diriwachter, G. 1985. Etude de la resistance croisee au metalaxyl et un cyprofurame chez Plasmopora viticola: Evidence de plusiers macanismes de resistance independants. p. 303306 in Smith, I. M., ed. Fungicides for Crop Protection—100 Years of Progress. Vol. 2. BCPC Publications, Croyden, U.K. Google Scholar
9. Cohen, Y. and Levy, Y. 1990. Joint action of fungicides in mixtures: Theory and practice. Phytoparasitica 18:159169.Google Scholar
10. Couch, H. B. and Smith, B. D. 1991. Synergistic and antagonistic interactions of fungicides against Pythium aphanidermatum on perennial ryegrass. Crop Prot. 10:386390.Google Scholar
11. Crute, I. R. 1984. The integrated use of genetic and chemical methods for control of lettuce downy mildew (Bremia lactucae Regel). Crop Prot. 3:223241.Google Scholar
12. Crute, I. R. 1989. Lettuce downy mildew: A case study in integrated control. p. 3053 in Leonard, K. J. and Fry, W. E., eds. Plant Disease Epidemiology, Vol. 2. McGraw-Hill Publ. Co., New York.Google Scholar
13. Crute, I. R. 1992. The contribution of genetic studies to understanding fungicide resistance. p. 1902021. Denholm, Devonshire, A. L., and Hollomon, D. W. eds. Resistance '91—Achievements and Developments in Combating Pesticide Resistance. Elsevier Applied Science, London, U.K. Google Scholar
14. Crate, I. R. and Harrison, J. M. 1988. Studies on the inheritance of resistance to metalaxyl in Bremia lactucae and on the stability and fitness of field isolates. Plant Pathol. 37:231250.CrossRefGoogle Scholar
15. Davidse, L. C., Looijen, D., Turkensteen, L. J., and van der Waal, D. 1981. Occurrence of metalaxyl-resistant strains of Phytophthora infestons in Dutch potato fields. Neth. J. Plant Pathol. 87:6568.Google Scholar
16. Devey, J. P., Barlow, J. N., and Redbond, M. R. 1990. Effectiveness of cyproconazole, alone and in combinations, against a range of stem base and foliar diseases in winter wheat. Br. Crop Prot. Conf.—Pests and Dis. 1990. p. 801806.Google Scholar
17. de Waard, M. A. 1984. Negatively correlated cross-resistance and synergism as strategies in coping with fungicide resistance. Br. Crop Prot. Conf.—Pests and Dis. 1984. p. 573584.Google Scholar
18. de Waard, M. A. 1991. Fungicide resistance strategies in winter wheat in the Netherlands. p. 4860 in Denholm, I., Devonshire, A. L., and Hollomon, D. W., eds. Resistance '91—Achievements and Developments in Combating Pesticide Resistance. Elsevier Applied Science, London, U.K. Google Scholar
19. 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 Path. 88:99112.Google Scholar
20. de Waard, M. A. and van Nistelrooy, J.G.M. 1983. Negatively correlated cross-resistance to dodine in fenarimol resistant isolates of various fungi. Neth. J. Plant Pathol. 89:6773.Google Scholar
21. 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. 96:321329.Google Scholar
22. Dekker, J. 1982. Introduction. p. 16 in Dekker, J. and Georgopoulos, S. G., eds. Fungicide Resistance in Crop Protection. Pudoc, Wagengingen, Netherlands.Google Scholar
23. Delp, C. J. 1980. Coping with resistance to plant disease control agents. Plant Dis. 64:52657.Google Scholar
24. Doster, M. A. and Fry, W. E. 1991. Evaluation by computer simulation of strategies to time metalaxyl applications for improved control of potato late blight. Crop Prot. 10:209214.Google Scholar
25. Elad, Y., Shabi, E., and Katan, T. 1988. Negative cross resistance between benzimidazole and N-phenylcarbamate fungicides and control of Botrytis cinerea on grapes. Plant Pathol. 37:141147.Google Scholar
26. Elad, Y., Yunis, H., and Katan, T. 1992. Multiple fungicide resistance to benzimidazoles, dicarboximides and diethofencarb in field isolates of Botrytis cinerea in Israel. Plant Pathol. 41:4146.Google Scholar
27. Enisz, J. 1988. Variation in sensitivity of Elysiphe graminis f.sp. tritici to SBI fungicides in western Hungary. Br. Crop Prot. Conf.—Pests and Dis. 1988. p. 373378.Google Scholar
28. Ennos, R. A. and Swales, K. W. 1991. Genetic variation in a fungal pathogen: Response to host defensive chemicals. Evolution 45:190234.Google Scholar
29. Falconer, D.S. 1989. Introduction to Quantitative Genetics. 3rd ed. Longman Scientific & Technical, New York, NY. 438 p.Google Scholar
30. Faretra, F., Pollastro, S., and Tonno, A. P. 1989. New natural variants of Botryotinia fuckeliana (Botrytis cinerea) coupling benzimidazole resistance to insensitivity toward the N-phenylcarbamate, diethofencarb. Phytopathol. Mediterr. 28:98104.Google Scholar
31. Fry, W. E. 1978. Quantification of general resistance of potato cultivars and fungicide effects for integrated control of potato late blight. Phytopathology 68:16501655.Google Scholar
32. Fry, W. E. 1987. Advances in disease forecasting. p. 239252 in Brent, K. J. and Atkin, R. K., eds. Rational Pesticide Use. Cambridge University Press, Cambridge, U.K. Google Scholar
33. Fry, W. E. and Milgroom, M. G. 1990. Population biology and management of fungicide resistance. p. 275285 in Green, M. B., LeBaron, H. M., and Moberg, W. K., eds. Managing Resistance to Agrochemicals—From Fundamental Research to Practical Strategies. ACS Press, Washington, D.C. CrossRefGoogle Scholar
34. Fuchs, A. and de Waard, M. A. 1982. Resistance to ergosterol biosynthesis inhibitors 1: Chemistry and phenomenological aspects. p. 7186 in Dekker, J. and Georgopoulos, S. G., eds. Fungicide Resistance in Crop Protection. Pudoc, Wageningen, Netherlands.Google Scholar
35. Gareth-Jones, D., Paveley, N. D., and Glover, M. A. 1985. Cultivar/fungicide interactions in the resistance of wheat to Septoria nodorum. Fungicides for Crop Protection. Vol. 2. BCPC Publications, Croyden, U.K. p. 355358.Google Scholar
36. Georgopoulos, S. G. 1977. Development of fungal resistance to fungicides. p. 439495 in Siegel, M. R. and Sisler, H. D., eds. Antifungal Compounds, Vol. 2. Marcell Dekker, New York.Google Scholar
37. Georgopoulos, S. G. 1982. Case Study I: Cercospora beticola of sugar beets. p. 187194 in Dekker, J. and Georgopoulos, S. G., eds. Fungicide Resistance in Crop Protection. Pudoc, Wageningen, Netherlands.Google Scholar
38. Georgopoulos, S. G. 1985. The genetic classification of fungicides according to resistance risk. EPPO Bull. 15:513517.Google Scholar
39. Girling, I. J., Hollomon, D. W., Kendall, S. J., Loeffler, R.S.T., and Senior, I. J. 1988. Effects of fenpropidin on DMI-resistant strains of Erysiphe graminis f.sp. hordei and Rhynchosporium secalis . Br. Crop Prot. Conf.—Pests and Dis. 1988. p. 385390.Google Scholar
40. Goodwin, S. B., Saghai-Maroof, M. A., Allard, R. W., and Webster, R. K. 1993. Isozyme variation within and among populations of Rhynchosporium secalis in Europe, Australia and the United States. Mycol. Res. 97:4958.Google Scholar
41. Grabski, C. and Gisi, U. 1987. Quantification of synergistic interactions of fungicides against Plasmopora and Phytophthora . Crop Prot. 6:6471.CrossRefGoogle Scholar
42. Heaney, S. P., Martin, T. J., and Smith, J. M. 1988. Practical approaches to managing anti-resistance strategies with DMI fungicides. Br. Crop Prot. Conf.—Pests and Dis. 1988. p. 10971106.Google Scholar
43. Hildebrand, P. D., Lockhart, C. L., Newberry, R. J., and Ross, R. G. 1988. Resistance of Venturia inaequalis to bitertanol and other demethylation-inhibiting fungicides. Can. J. Plant Pathol. 10:311316.Google Scholar
44. Hollomon, D. W. 1986. Contribution of fundamental research to combating resistance. Br. Crop Prot. Conf.—Pests and Dis. 1986. p. 801810.Google Scholar
45. Horsten, J. and Fehrmann, H. 1980. Fungicide resistance of Septona nodorum and Pseudocercosporella herpotnchoides III: Survival ability of resistant strains in mixed populations. Z. fur Pflanzenkr. Pflanzenschutz 87:577586.Google Scholar
46. Hsiang, T. and Chastagner, G. A. 1991. Growth and virulence of fungicide-resistant isolates of three species of Botrytis . Can. J. Plant Pathol. 13:226231.Google Scholar
47. Ishii, H., Udagawa, H., Yanase, H., and Yamaguchi, A. 1985. Resistance of Venturia nashicola to thiophanate-methyl and benomyl: Build-up and decline of resistance in the field. Plant Pathol. 34:363368.Google Scholar
48. Jones, A. L. 1981. Fungicide resistance: Past experience with benomyl and dodine and future concerns with sterol inhibitors. Plant Dis. 65:990992.Google Scholar
49. Jorgerisen, L. N. and Nielsen, B. J. 1992. Reduced dosages of fungicides for controlling wheat-diseases in Denmark. Br. Crop Prot. Conf.—Pests and Dis. 1992. p. 609614.Google Scholar
50. Josepovits, G. and Dobrovolszky, A. 1985. A novel mathematical approach to the prevention of fungicide resistance. Pestic. Sci. 16:1722.Google Scholar
51. Kable, P. F. and Jeffery, H. 1980. Selection for tolerance in organisms exposed to sprays of biocide mixtures: A theoretical model. Phytopathology 70:812.Google Scholar
52. Kadish, D. and Cohen, Y. 1988. Fitness of Phytophthora infestans isolates from metalaxyl-sensitive and resistant populations. Phytopathology 78:912915.Google Scholar
53. Katan, T. and Bashi, E. 1981. Resistance to metalaxyl in an isolate of Pseudoperonospora cubensis, the downy mildew of cucurbit. Plant Dis. 65:798800.Google Scholar
54. Katan, T., Elad, Y., and Yunis, H. 1989. Resistance to diethofencarb (NPC) in benomyl-resistant field isolates of Botrytis cinerea . Plant Pathol. 38:8692.Google Scholar
55. Kato, T., Suzuki, K., Takahashi, J., and Kamoshita, K. 1984. Negatively correlated cross resistance between benzimidazole fungicides and methyl N-3,5-dichlorophenyl-carbamate. Jpn. Pestic. Sci. 9:489495.CrossRefGoogle Scholar
56. Kendall, S. J. 1986. Cross-resistance of triadimenol-resistant fungal isolates to other sterol C-14 demethylation inhibitor fungicides. Br. Crop Prot. Conf.—Pests and Dis. 1986. p. 539546.Google Scholar
57. Kendall, S. J. and Hollomon, D. W. 1990. DMI resistance and sterol demethylation in Rhynchosporium secalis . Br. Crop Prot. Conf.—Pests and Dis. 1990. p. 11291134.Google Scholar
58. Koenraadt, H., Somerville, S. C., and Jones, A. L. 1992. Characterization of mutations in the beta-tubulin gene of benomyl-resistant field strains of Venturia inaequalis and other plant pathogenic fungi. Phytopathology 82:13481354.Google Scholar
59. Köller, W. and Scheinpflug, H. 1987. Fungal resistance to sterol biosynthesis inhibitors: a new challenge. Plant Dis. 71:10661074.Google Scholar
60. Lalancette, N., Hickey, K. D., and Cole, H. Jr. 1987. Parasitic fitness and intrastrain diversity of benomyl-sensitive and benomyl-resistant subpopulations of Venturia inaequalis . Phytopathology 77:16001606.Google Scholar
61. Leroux, P. 1992. Negative cross resistance in fungicides: From the laboratory to the field. p. 179187 in Denholm, I., Devonshire, A. L., and Hollomon, D. W., eds. Resistance '91—Achievements and Developments in Combating Pesticide Resistance. Elsevier Applied Science, London, U.K. Google Scholar
62. Levy, Y., Levi, R., and Cohen, Y. 1983. Buildup of a pathogen subpopulation resistant to a systemic fungicide under various control strategies: A flexible simulation model. Phytopathology 73:14751480.Google Scholar
63. Lorenz, G., Saur, R., and Schelberger, K. 1992. Long term monitoring results of wheat powdery mildew sensitivity towards fenpropimorph and strategies to avoid the development of resistance. Br. Crop Prot. Conf.—Pests and Dis. 1992. p. 171176.Google Scholar
64. Maloy, O. C. 1993. Plant Disease Control—Principles and Practice. John Wiley and Sons Inc., New York, U.S.A. 346 p.Google Scholar
65. McDermott, J. M. and McDonald, B. A. 1993. Gene flow in plant pathosystems. Annu. Rev. Phytopathol. 31:353373.Google Scholar
66. McKenzie, J. A., Whitten, M. J., and Adena, M. A. 1982. The effect of genetic background on the fitness of diazinon resistance in the Australian sheep blowfly, Lucilia cuprina . Heredity 49:19.Google Scholar
67. Milgroom, M. G. 1990. A stochastic model for the initial occurrence and development of fungicide resistance in plant pathogen populations. Phytopathology 80:410416.Google Scholar
68. Milgroom, M. G. and Fry, W. E. 1988. A simulation analysis of the epidemiological principles for fungicide resistance management in pathogen populations. Phytopathology 78:565570.Google Scholar
69. Milgroom, M. G., Levin, S. A., and Fry, W. E. 1989. Population genetics theory and fungicide resistance. p. 341367 in Leonard, K. J. and Fry, W. E., eds. Plant Disease Epidemiology, Vol. 2. McGraw-Hill Publ. Co., New York.Google Scholar
70. Milgroom, M. G., Lipari, S. E., Ennos, R. A., and Liu, Y. C. 1993. Estimation of the outcrossing rate in the chestnut blight fungus, Cryphonectria parasitica . Heredity 70:385392.Google Scholar
71. Miyagi, Y., Hirooka, T., and Araki, F. 1986. Relative parasitic fitness of isolates of Pyricularia oryzae Cav. with different sensitivities to fungicides. Pestic. Sci. 17:653658.Google Scholar
72. Nathaniels, N.Q.R., Wilson, K., and Fletcher, J. T. 1985. Negative cross resistance between benomyl and MDPC in British isolates of Botrytis cinerea, Pseudocercosporella herpotrichoides and Verticillium fungicola var. fungicola. Ann. Appl. Biol. 107:151154.Google Scholar
73. Nuninger-Ney, C., Schwinn, F. J., and Staub, T. 1989. In vitro selection of sterol-biosynthesis inhibitor (SBI)-resistant mutants in Monilinia fructicola (Wint.) Honey. Neth. J. Plant Pathol. 95 (Suppl. 1): 137150.Google Scholar
74. Peever, T. L. and Milgroom, M. G. 1992. Inheritance of triadimenol resistance in Pyrenophora teres . Phytopathology 82:821828.Google Scholar
75. Peever, T. L. and Milgroom, M. G. 1993. Genetic correlations in resistance to sterol biosynthesis-inhibiting fungicides in Pyrenophora teres . Phytopathology 83:10761082.Google Scholar
76. Peever, T. L. and Milgroom, M. G. 1994. Lack of correlation between fitness and resistance to sterol biosynthesis inhibiting fungicides in Pyrenophora teres . Phytopathology 84:515519.Google Scholar
77. Peever, T. L. and Milgroom, M. G. 1994. Genetic structure of Pyrenophora teres populations determined with RAPD markers. Can. J. Bot. 72:915923.Google Scholar
78. Robertson, S., Gilmour, J., Newman, D., and Lennard, J. H. 1990. Sensitivity of barley powdery mildew isolates to morpholine fungicides. Br. Crop Prot. Conf.—Pests and Dis. 1990. p. 11591162.Google Scholar
79. Samoucha, Y. and Cohen, Y. 1988. Synergistic interactions of cymoxanil mixtures in the control of metalaxyl-resistant Phytophthora infestans of potato. Phytopathology 78:636640.Google Scholar
80. Sanders, P. L., Houser, W. J., Pansh, P. J., and Cole, H. Jr. 1985. Reduced-rate fungicide mixtures to delay fungicide resistance and to control selected turfgrass diseases. Plant Dis. 69:939943.Google Scholar
81. Schepers, H. T. A. M. 1983. Decreased sensitivity of Sphaerotheca fuliginea to fungicides which inhibit ergosterol biosynthesis. Neth. J. Plant Pathol. 89:185187.Google Scholar
82. Schwinn, F. and Morton, H. 1990. Antiresistance Strategies—Design and implementation in practice. p. 170183 in Green, M. B., LeBaron, H. M., and Moberg, W. K., eds. Managing Resistance to Agrochemicals—From Fundamental Research to Practical Strategies. ACS Press, Washington, D.C. Google Scholar
83. Shaw, M. W. 1989. A model of the evolution of polygenically controlled fungicide resistance. Plant Pathol. 38:4455.Google Scholar
84. Shaw, M. W. 1989. Independent action of fungicides and its consequences for strategies to retard the evolution of fungicide resistance. Crop Prot. 8:405411.Google Scholar
85. Shaw, M. W. 1993. Theoretical analysis of the effect of interacting activities on the rate of selection for combined resistance to fungicide mixtures. Crop Prot. 12:120126.Google Scholar
86. Skylakakis, G. 1981. Effects on alternating and mixing pesticides on the buildup of fungal resistance. Phytopathology 71:11191121.Google Scholar
87. Skylakakis, G. 1982. Epidemiological factors affecting the rate of selection of biocide-resistant genotypes of plant pathogenic fungi. Phytopathology 72:271273.Google Scholar
88. Smilanick, J. L. and Eckert, J. W. 1986. Growth, sporulation and virulence of isolates of Penicillium digitatum resistant to the fungicide sec-butylamine. Phytopathology 76:805808.Google Scholar
89. Staub, T. 1991. Fungicide resistance: Practical experience with antiresistance strategies and the role of integrated use. Annu. Rev. Phytopathol. 29:421442.Google Scholar
90. Staub, T. and Sozzi, D. 1983. Recent practical experiences with fungicide resistance. Proc. 10th Int. Cong. Plant Prot. p. 591598.Google Scholar
91. Stott, I.P.H., Noon, R. A., and Heaney, S. P. 1990. Flutriafol, ethirimol and thiabendazole seed treatment—An update on field performance and resistance monitoring. Br. Crop Prot. Conf.—Pests and Dis. 1990. pp. 11691174.Google Scholar
92. Thind, T. S., Clerjeau, M., and Olivier, J. M. 1986. First observations on resistance in Venturia inaequalis and Guignardia bidwellii to ergosterol-biosynthesis inhibitors in France. Br. Crop Prot. Conf.—Pests and Dis. 1986. p. 491498.Google Scholar
93. Uyenoyama, M. K. 1986. Pleiotropy and the evolution of genetic systems conferring resistance to pesticides. p. 207221 in Strategies and Tactics for Management. National Academy Press, Washington, D.C. Google Scholar
94. Via, S. 1984. The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants. Evolution 38:896905.Google Scholar
95. Via, S. 1986. Quantitative genetic models and the evolution of pesticide resistance. p. 222235 in Pesticide Resistance: Strategies and Tactics for Management. National Academy Press, Washington, DC.Google Scholar
96. Webber, J. F. 1988. Effect of MBC fungicide tolerance on the fitness of Ophiostoma ulmi . Plant Pathol. 37:217224.Google Scholar
97. Wicks, T. 1974. Tolerance of the apple scab fungus to benzimidazole fungicides. Plant Dis. Rep. 58:886889.Google Scholar
98. Wolfe, M. S. 1984. Trying to understand and control powdery mildew. Plant Pathol. 33:451466.Google Scholar
99. Yarden, O. and Katan, T. 1993. Mutations leading to substitutions at amino acids 198 and 200 of beta-tubulin that correlate with benomyl-resistance phenotypes of field strains of Botrytis cinerea . Phytopathology 83:14781483.Google Scholar
100. Yuen, J. E. and Lorbeer, J. W. 1983. Metalaxyl controls downy mildew and supplements horizontal resistance to Bremia lactucae in lettuce grown on organic soil in New York. Plant Dis. 66:615618.Google Scholar