Problems of Fungicide Resistance in Penicillium Rot of Citrus Fruits

  • Joseph W. Eckert
  • Brian L. Wild

Abstract

Green and blue mold of citrus fruits are incited by the ubiquitous fungi Penioillium digitatum Sacc. and P. italioum Wehm., respectively. Green mold is the most important cause of postharvest decay of citrus fruits produced in areas with scant rainfall during the period of fruit maturation. Blue mold is of lesser overall importance, but may become the major problem under environmental conditions or fungicide treatments that selectively suppress the development of green mold. Penicillium molds are also important in humid production areas but tend to be overshadowed there by the stem-end rots. In nature, P. digitatum completes its life cycle only on citrus fruits, whereas P. italioum can infect an array of different fruits and vegetables. Spores of P. digitatum and P. italioum that form on diseased fruits on the ground in citrus groves and in packinghouses are transported by air currents to healthy fruits. The surface of virtually every citrus fruit is contaminated with these spores at harvest time, but they are unable to germinate and infect the fruit except at injury sites, where the rate of infection reaches a maximum at about 25°C under high humidity conditions. Infected fruit are decayed totally within 7 days and the fungus sporulates heavily on the fruit surface.

Keywords

Mold Fusarium Carben Thiophanate Carbamate 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bartz, J. A., and Eckert, J. W., 1972, Studies on the mechanism of action of 2-aminobutane, Phytopathology, 62:239.CrossRefGoogle Scholar
  2. Beraha, L., and Garber, E. D., 1965, Genetics of phytopathogenic fungi. XI. A genetic study of avirulence due to auxotrophy in Penicillium expansion. Am. J. Bot., 52:117.CrossRefGoogle Scholar
  3. Beraha, L., and Garber, E.D., 1966, Genetics of phytopathogenic fungi. XV. A genetic study of resistance to sodium ortho-phenylphenate and sodium dehydroacetate in Penicillium expansum, Am. J. Bot., 53:1041.CrossRefGoogle Scholar
  4. Beraha, L., and Garber, E. D., 1980, A genetic study of resistance to thiabendazole and sodium O-phenylphenate in Penicillium italicum by the parasexual cycle, Botan. Gaz., 141:204.CrossRefGoogle Scholar
  5. Beraha, L., Garber, E. D., and Strømnaes, O., 1964, Genetics of phytopathogenic fungi. X. Virulence of color and nutritionally deficient mutants of Pénicillium italicum and Penicillium digitatum, Can. J. Bot., 42:429.CrossRefGoogle Scholar
  6. Bertrand, P. F., and Saulie-Carter, J. L., 1978, The occurrence of benomyl-tolerant strains of Penicillium expansion and Botrytis cinerea in the mid-Columbia region of Oregon and Washington, Plant Disease Reptr., 62:302.Google Scholar
  7. Bollen, G. J., 1971, Resistance to benomyl and some chemically related compounds in strains of Penicillium species, Neth. J. Pl. Pathol., 77:187.CrossRefGoogle Scholar
  8. Brown, G. E., 1977, Application of benzimidazole fungicides for citrus decay control, Proc. Int. Soc. Citric, 1:273.Google Scholar
  9. Buchenauer, H., 1977, Mechanism of action of the fungicide imazalil in Ustilago avenae, Z. Pflccnzerikrarikr. u. Pflanzenschutz., 84:440.Google Scholar
  10. Chastagner, G. A., and Ogawa, J. M., 1979, DCNA-benomyl multiple tolerance in strains of Botrytis cinerea, Phytopathology, 69:699.CrossRefGoogle Scholar
  11. Davidse, L. C., 1973, Antimitotic activity of methyl benzimidazole-2-yl carbamate (MBC) in Aspergillus nidulans, Pestic. Biochem. Physiol., 3:317.CrossRefGoogle Scholar
  12. Davidse, L. C., 1976, The antimitotic properties of the benzimidazole fungicide carbendazim and a mechanism of resistance to this compound in Aspergillus nidulans, Doctoral Thesis, Agricultural University, Wageningen, Netherlands, 84 pp.Google Scholar
  13. Davidse, L. C., 1977, Mode of action, selectivity and mutagenicity of benzimidazole compounds., Neth. J. Pl. Pathol., 83(Suppl. 1): 135.CrossRefGoogle Scholar
  14. Davidse, L. C., and Flach, W., 1977, Differential binding of methyl benzimidazole-2-yl carbamate to fungal tubulin as a mechanism of resistance to this antimitotic agent in mutant strains of Aspergillus nidulans, J. Cell. Biol., 72:174.PubMedCrossRefGoogle Scholar
  15. Dawson, A. J., and Eckert, J. W., 1977, Problems of decay control in marketing citrus fruits: Strategy and solutions, California and Arizona, Proc. Int. Soc. Citric, 1:255.Google Scholar
  16. Dekker, J., 1977, The fungicide-resistance problem, Neth. J. Pl. Pathol., 83(Suppl. 1):159.CrossRefGoogle Scholar
  17. Duran, R., and Norman, S. M., 1961, Differential sensitivity to biphenyl among strains of Penicillium digitatum Sacc, Plant Disease Reptr., 45:475.Google Scholar
  18. Eckert, J. W., 1977, Control of postharvest diseases, in: “Antifungal Compounds,” M. R. Siegel and H. D. Sisler, eds., Vol. 1, pp. 269–352, Marcel Dekker Inc., New York.Google Scholar
  19. Eckert, J. W., 1978, Postharvest diseases of citrus fruits, Outlook on Agric, 9:225.Google Scholar
  20. Eckert, J. W., and Rahm, M. L., 1979, The antifungal activity of alkyl benzimidazole-2-yl carbamates and related compounds, Pestic. Sci., 10:473.CrossRefGoogle Scholar
  21. Eckert, J. W., Kolbezen, M. J., Rahm, M. L., and Eckard, K. J., 1979, Influence of benomyl and methyl 2-benzimidazolecarbamate on development of Penicillium digitatum in the precarp of orange fruit, Phytopathology, 69:934.CrossRefGoogle Scholar
  22. Farkas, A., and Aman, J., 1940, The action of diphenyl on Penicillium and Diplodia moulds, Palestine J. Bot. Jerusalem Ser.., 2:38.Google Scholar
  23. Georgopoulos, S. G., 1977, Development of fungal resistance to fungicides, in: “Antifungal Compounds,” M. R. Siegel and H. D. Sisler, eds., Vol 2, pp. 439–495, Marcel Dekker Inc., New York.Google Scholar
  24. Georgopoulos, S. G., Zafiratos, C., and Georgiadis, E., 1967, Membrane functions and tolerance to aromatic fungitoxicants in conidia of Fusarium solani, Physiol. Plant., 20:373.CrossRefGoogle Scholar
  25. Georgopoulos, S. G., Kappas, A., and Hastie, A. C., 1976, Induced sectoring in diploid Aspergillus nidulans as a criterion of fungitoxicity by interference with hereditary processes, Phytopatho logy, 66:217.Google Scholar
  26. Georgopoulos, S. G., Sarris, M., and Ziogas, B. M., 1979, Mitotic instability in Aspergillus nidulans caused by the fungicides iprodione, procymidone and vinclozolin, Pestic. Sci., 10:389.CrossRefGoogle Scholar
  27. Greenaway, W., Ward, S., and Whatley, F. R., 1978, Uptake of fuberi-dazole and thiabendazole by Penicillium digitatum, Cunningham-ella echinulata and potato slices, New Phytol., 80:595.CrossRefGoogle Scholar
  28. Gutter, Y., 1975, Interrelationship of Penicillium digitatum and P. italicum in thiabendazole-treated oranges, Phytopathology, 65:498.CrossRefGoogle Scholar
  29. Hammerschlag, R. S., and Sisler, H. D., 1973, Benomyl and methyl-2-benzimidazolecarbamate (MBC): Biochemical, cytological and chemical aspects of toxicity to Ustilago may dis and Saccharomyces cerevisiae, Pestic. Biochem. Physiol., 3:42CrossRefGoogle Scholar
  30. Harding, P. R., Jr., 1962, Differential sensitivity to sodium orthophenylphenate by biphenyl-sensitive and biphenyl-resistant strains of Penicillium digitatum, Plant Disease Reptr., 46:100.Google Scholar
  31. Harding, P. R., Jr., 1964, Assaying for biphenyl resistance in Penicillium digitatum in California lemon packing houses, Plant Disease Reptr., 48:43.Google Scholar
  32. Harding, P. R., Jr., 1965, The nature of biphenyl-resistant mutants of Penicillium digitatum, Plant Disease Reptr., 49:965.Google Scholar
  33. Harding, P. R., Jr., 1972, Differential sensitivity to thiabendazole by strains of Penicillium italicum and P. digitatum, Plant Disease Reptr., 56:256.Google Scholar
  34. Harding, P. R. Jr., 1976, R23979, a new imidazole derivative effective against postharvest decay of citrus by molds resistant to thiabendazole, benomyl and 2-aminobutane, Plant Disease Reptr., 60:643.Google Scholar
  35. Hastie, A. C., and Georgopoulos, S. G., 1971, Mutational resistance to fungitoxic benzimidazole derivatives in Aspergillus nidulans, J. Gen. Microbiol., 67:371.PubMedGoogle Scholar
  36. Herbig, G., and Rehm, J.-J., 1967, Stoffwechsel-physiologische Untersuchungen en diphenyl-und natrim-O-phenyl-phenolatresistenten Pilzen., Naturiwiss., 54, 46.CrossRefGoogle Scholar
  37. Houck, L. G., 1977, Problems of resistance to citrus fungicides, Proc. Int. Soc. Citric., 1:263.Google Scholar
  38. Koffmann, W., Penrose, L. J., Menzies, A. R., Davis, K. C., and Kaldor, J., 1978, Control of benzimidazole tolerant Penicillium expansion in pome fruit, Sci. Hortic, 9:31.CrossRefGoogle Scholar
  39. Kuramoto, T., 1976, Resistance to benomyl and thiophanate-methyl in strains of Penicillium digitatum and P. italicum in Japan, Plant Disease Reptr., 60:168.Google Scholar
  40. Laville, E. Y., Harding, P. R., Dagan, Y., Rabat, M., Kragbt, A. J., and Rippon, L. E., 1977, Studies on imazalil as a potential treatment for control of citrus fruit decay, Proc. Int. Soc. Citric, 1:269.Google Scholar
  41. Leroux, P., and Gredt, M., 1978, Effets de quelques fongicides systemiques sur la biosynthêse de l’ Ertostérol chez Botrytis cinerea Pers., Penicillium expansum Link, et Ustilago maydis (DC.) Cda. Ann. Phytopathology, 10:45.Google Scholar
  42. Littauer, F., and Gutter, Y., 1953, Diphenyl-resistant strains of Diplodia, Palestine J. Bot., Rehovot Ser., 8:185.Google Scholar
  43. McDonald, R. E., Risse, L. A., Hillebrand, B. M., 1979, Resistance to thiabendazole and benomyl of Penicillium digitatum and P. italicum isolated from citrus fruit from several countries, J. Am. Soc. Hort. Sci., 104:333.Google Scholar
  44. Muirhead, I. F., 1974, Resistance to benzimidazole fungicides in blue mould of citrus in Queensland, Australian J. Exptl. Agr. Animal Husbandry, 14:698.CrossRefGoogle Scholar
  45. Nachmias, A., and Barash, I., 1976, Decreased permeability as a mechanism of resistance to methyl benzimidazol-2-yl carbamate (MBC) in Sporobolomyces roseus, J. Gen. Microbiol., 94:167.PubMedGoogle Scholar
  46. Rehm, H.-J., 1969, Inhibiting action of sodium O-phenylphenate (SOPP) and biphenyl on specific reactions of the metabolism of microorganisms, Proc. First Int. Citrus Symp., 3:1325.Google Scholar
  47. Rosenberger, D. A., and Meyer, F. W., 1979, Benomyl-tolerant Penicillium expansum in apple packinghouses in Eastern New York, Plant Disease Reptr., 63:37.Google Scholar
  48. Rosenberger, D. A., Meyer, F. W., and Cecilia, C. V., 1979, Fungicide strategies for control of benomyl-tolerant Penicillium expansum in apple storages, Plant Disease Reptr., 63:1033.Google Scholar
  49. Siegel, M. R., and Ragsdale, N. N., 1978, Antifungal mode of action of imazalil, Pestic. Biochem. Physiol., 9:48.CrossRefGoogle Scholar
  50. Smoot, J. J., and Brown, G. E., 1974, Occurrence of benzimidazole-resistant strains of Penicillium digitatum in Florida citrus packinghouses, Plant Disease Reptr., 58:933.Google Scholar
  51. Smoot, J. J., and Winston, J. R., 1967, Biphenyl-resistant citrus green mold reported in Florida, Plant Disease Reptr., 51:700.Google Scholar
  52. Strømnaes, O., Garber, E. D., and Beraha, L., 1964, Genetics of phytopathogenic fungi. IX. Heterocaryosis and the parasexual cycle in Penicillium italicum and P. digitatum, Can. J. Bot., 42:423.CrossRefGoogle Scholar
  53. Sutton, T. B., 1978, Failure of combinations of benomyl and reduced rates of non-benzimidazole fungicides to control Venturia inaequalis resistant to benomyl and the spread of resistant strains in North Carolina, Fiant Disease Reptr., 62:830.Google Scholar
  54. Uesugi, Y., 1981, this volume.Google Scholar
  55. Van Tuyl, J. M., 1975, Genetic aspects of acquired resistance to benomyl and thiabendazole in a number of fungi, Med. Fac. Landbouw. Rijksuniv. Gent., 40:691.Google Scholar
  56. Van Tuyl, J. M., 1977a, Genetic aspects of resistance to imazalil in Aspergillus nidulans, Neth. J. Fl. Pathol., 83(Suppl. 1):169.CrossRefGoogle Scholar
  57. Van Tuyl, J. M., 1977b, Genetics of fungal resistance to systemic fungicides, Doctoral Thesis, Agricultural University, Wageningen, Netherlands, 137 pp.Google Scholar
  58. Vonk, J. W., and Kaars Sijpesteijn, A., 1971, Methyl benzimidazole-2-yl carbamate, the fungitoxic principle of thiophanate-methyl, Festic. Sci., 2:160.CrossRefGoogle Scholar
  59. Wicks, T., 1977, Tolerance to benzimidazole fungicides in blue mold (Penicillium expansum) on pears, Plant Disease Reptr., 61:447.Google Scholar
  60. Wild, B. L., 1980, Resistance to citrus green mold Penicillium digitatum Sacc. to benzimidazole fungicides, Doctoral Thesis, University of California, Riverside, 89 pp.Google Scholar
  61. Wild, B. L., and Rippon, L. E., 1975, Response of Penicillium digitatum strains to benomyl, thiabendazole and sodium O-phenylphenate, Phytopathology 3 65:1176.CrossRefGoogle Scholar
  62. Wolfe, M. S., 1971, Fungicides and the fungus population problem, Proc. 6th Brit. Insectic. Fungic. Conf., 3:724.Google Scholar
  63. Wolfe, M. S., 1975, Pathogen response to fungicide use, Proc. 8th Brit. Insectic. Fungic. Conf., 3:813.Google Scholar
  64. Yoshikawa, M., and Eckert, J. W., 1976, The mechanism of fungistatic action of sec-hutylamine. I. Effects of sec-butylamine on the metabolism of hyphae of Penicillium digitatum, Pestic. Biochem. Physiol.., 6:471.CrossRefGoogle Scholar
  65. Yoshikawa, M., Eckert, J. W., and Keen, N. T., 1976, The mechanism of fungistatic action of sec-butylamine. II. The effect of sec-butylamine on pyruvate oxidation by mitochondria of Penicillium digitatum and on the pyruvate dehydrogenase complex, Pestic. Biochem. Physiol., 6:482.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1983

Authors and Affiliations

  • Joseph W. Eckert
    • 1
  • Brian L. Wild
    • 1
  1. 1.Department of Plant PathologyUniversity of CaliforniaRiversideUSA

Personalised recommendations