Sensitivity of Penicillium digitatum isolates, causal agent of citrus green mold, to imazalil, fludioxonil, pyrimethanil, azoxystrobin and thiabendazole in Northof Iran

Document Type : Complete scientific research article

Authors

1 Islamic Azad University, Gorgan Branch, Gorgan, Iran

2 Department of Plant Protection Research, Agriculture and Natural Resources Research and Education Center of Golestan Province, Gorgan, Iran

Abstract

Green mold is the most common post-harvest disease of citrus which is caused by the fungus Penicillium digitatum. In order to evaluate the effectiveness of post-harvest citrus fungicides in terms of inhibiting mycelium growth and conidial germination, 150 samples were randomly sampled from the warehouses and orchards of three eastern (Gorgan region), central (Sari and Ghaemshahr) and western (Ramsar and Tonkabon) sites and 15 fungal isolates were extracted from them. The results of the laboratory studies showed that the lowest to the highest average values of EC50 for the growth of mushroom mycelium were related to the fungicides Azoxystrobin, Imazalil, Fludioxonil, Pyrimetanil and Thiabendazole with the values of 0.045, 0.065, 0.08, 0.34 and 0.55 μg/ml, and for inhibiting the germination of conidia. respectively, from the lowest to the highest average EC50 values, related to azoxystrobin, imazalil, fludioxonil, thiabendazole and pyrimethanil with values of 0.072, 0.117, 0.155, 0.731 and 0.774 µg/ml. All isolates were sensitive to the fungicide Azoxystrobin, but the EC50 values were outside the baseline range. Also, all isolates were sensitive to fludioxonil fungicide and some isolates had EC50 values outside the baseline range. The EC50 values of all the isolates were in the sensitive range to the fungicide imazalil, and in relation to the fungicide pyrimethanil, all the isolates were sensitive and some isolates were outside the basic range. Four isolates were resistant to thiabendazole fungicide and 11 isolates were in the sensitive range.
Green mold is the most common post-harvest disease of citrus which is caused by the fungus Penicillium digitatum. In order to evaluate the effectiveness of post-harvest citrus fungicides in terms of inhibiting mycelium growth and conidial germination, 150 samples were randomly sampled from the warehouses and orchards of three eastern (Gorgan region), central (Sari and Ghaemshahr) and western (Ramsar and Tonkabon) sites and 15 fungal isolates were extracted from them. The results of the laboratory studies showed that the lowest to the highest average values of EC50 for the growth of mushroom mycelium were related to the fungicides Azoxystrobin, Imazalil, Fludioxonil, Pyrimetanil and Thiabendazole with the values of 0.045, 0.065, 0.08, 0.34 and 0.55 μg/ml, and for inhibiting the germination of conidia. respectively, from the lowest to the highest average EC50 values, related to azoxystrobin, imazalil, fludioxonil, thiabendazole and pyrimethanil with values of 0.072, 0.117, 0.155, 0.731 and 0.774 µg/ml. All isolates were sensitive to the fungicide Azoxystrobin, but the EC50 values were outside the baseline range. Also, all isolates were sensitive to fludioxonil fungicide and some isolates had EC50 values outside the baseline range. The EC50 values of all the isolates were in the sensitive range to the fungicide imazalil, and in relation to the fungicide pyrimethanil, all the isolates were sensitive and some isolates were outside the basic range. Four isolates were resistant to thiabendazole fungicide and 11 isolates were in the sensitive range.

Keywords

Main Subjects


  1. Aquino, S., Schirra, M., Palma, A., & Liguori, R. (2008, November). Effectiveness of fludioxonil against Penicillium decay in citrus fruit. In III International Conference Postharvest Unlimited 2008 858 (pp. 357-362).
  2. Arras, G. (1996). Mode of action of an isolate of Candida famata in biological control of Penicillium digitatum in orange fruits. Postharvest Biology and Technology, 8(3): 191-198.
  3. Ballester, A. R., Lafuente, M. T., & González-Candelas, L. (2006). Spatial study of antioxidant enzymes, peroxidase and phenylalanine ammonia-lyase in the citrus fruit–Penicillium digitatum interaction. Postharvest Biology and Technology, 39(2), 115-124.
  4. H, Saadi.B, Boudyach.E and Benaoumar.A, 2009. Sensitivity of Penicillium digitatum and P. italicum to Imazalil and Thiabendazole in Morocco. Plant Pathology Journal, 8: 152-158.
  5. Brent, K. J. 1988. Monitoring for fungicide resistance. Pages 9-11 in: Fungicide resistance in North America. C. J. Delp, ed. American Phytopathological Society Press, St. Paul, MN.
  6. Bus, V. G. 1992. ED50 levels of Penicillium digitatum and P. italicum with reduced sensitivity to thiabendazole, benomyl, and imazalil. Postharv. Biol. Technol. 1:305-315
  7. California Agricultural Resource Directory, 2005. California Department of Food and Agriculture. Pages 179 (online publication: http://www.cdfa.ca.gov/card/pdfs/ agresdirentire05 .pdf).
  8. Crous PW, Gams W, Stalpers JA, Robert V and Stegehuis G, 2004. MycoBank: an online initiative to launch mycology into the 21st century. Studies in Mycology 50: 19-22.
  9. Dan, F. E. N. G., Xue-peng, S. U. N., Li-ying, J. I. A. N. G., Jian-min, C. H. E. N., & Hong-ye, L. I. (2011). Resistance level and mechanism of Penicillium digitatum to imazalil and carbendazim in Quzhou, Zhejiang. Chinese Journal of Pesticide Science, 13(4), 341-346.
  10. Del Río, J.A., Arcas, M.C., Benavente-García, O., & Ortuño, A. (1998). Citrus polymethoxylated flavones can confer resistance against Phytophthora citrophthora, Penicillium digitatum, and Geotrichum species. Journal of Agricultural and Food Chemistry, 46(10), 4423-4428.
  11. Eckert, J. W., & Wild, B. L. (1983). Problems of fungicide resistance in Penicillium rot of citrus fruits. In Pest Resistance to Pesticides (pp. 525-556). Boston, MA: Springer US.
  12. Eckert, J.W., Brown, G.E., 1986. Evaluation of postharvest fungicide treatments for citrusfruits. In: Hickey, K.D. (Ed.), Methods for Evaluating Pesticides for Control of PlantPathogens. APS Press, St Paul, MN, USA, pp. 92–97.
  13. Eckert, J.W., Eaks, I.L., 1989. Postharvest disorders and diseases of citrus fruits. In: Reuter, W., Calavan, E.C., Carman, G.E. (Eds.), The Citrus Industry. DANR. University of California Press, Berkeley, CA, USA, pp. 179–260.
  14. Eckert, J.W., Ratnayake, M., 1994. Role of volatile compounds from wounded oranges ininduction of germination of Penicillium digitatum conidia. Phytopathology, 84: 746–750.
  15. Erasmus, A., Lennox, C.L., Jordaan, H., Smilanick, J.L., Lesar, K., and Fourie, P.H. 2011. Imazalil residue loading and green mould control in citrus packhouses. Postharvest Biology and Technology, 62: 193–2
  16. Erasmus, A., Lennox, C.L., Korsten, L., Lesar, K., Fourie, P.H., 2015. Imazalil resistance in Penicillium digitatum and P. italicum causing citrus postharvest green and blue mould: impact and options. Postharvest Biology and Technology, 107: 66–76.
  17. 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.
  18. Fatahi Moghadam J., Golmohammadi M. 2012. A review of the effective activities in reducing the waste of citrus fruit harvest and after harvest. Citrus and Subtropical Fruits Research Institute, Iran. Extension booklet.
  19. Kanetis, L., Förster, H. and Adaskaveg, J.E. 2008. Baseline sensitivities for new postharvest fungicides against Penicillium spp. on citrus and multiple resistance evaluations in Penicillium digitatum. Plant Disease, 92: 301–310.
  20. Kanetis, L., Förster, H. and Adaskaveg, J.E. 2010. Determination of natural resistance frequencies in Penicillium digitatum using a new air-sampling method and characterization of fludioxonil- and pyrimethanil-resistant isolates. Phytopathology 100: 738–746.
  21. Kanetis, L., Förster, H., Adaskaveg, J.E., 2007. Comparative efficacy of the new postharvest fungicides Azoxystrobin, Fludioxonil, and Pyrimethanil for managing citrus green mold. Plant Disease 91: 1502–1511
  22. Kendall Brent, & Hollomon, D. W. (1998). Fungicide resistance: the assessment of risk (Vol. 2). Brussels, Belgium: Global Crop Protection Federation.
  23. Kinay, P., Mansour, M.F., Mlikota-Gabler, F., Margosan, D.A., Smilanick, J.L. 2007. Charac­terization of fungicide-resistant isolates of Penicillium digitatum collected in California. Crop Protection 26: 647–656.
  24. Louw, J. P. & Korsten, L. 2015. Pathogenicity and host susceptibility of Penicillium spp. on citrus. Plant Disease 99(1): 21–30.
  25. Pandey, D. K., Tripathi, N. N., Tripathi, R. D., and Dixit, S. N. 1982. Fungitoxic and phytotoxic properties of the essential oil of Hyptissuaveolens/Fungitoxische und phytotoxischeEigenschaften des ätherischenÖis von Hyptissuaveolens. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz/Journal of Plant Diseases and Protection: 344-349.
  26. Patil,S. R., Parthiban, V.K., Sekar, G. R., and Baviskar, S. 2017: Epidemiology and cultural characteristics ofPenicillium digitatum causing green mould of citrus. Ecology, Environment and Conservation Paper 23 (4): 2148-2155.
  27. Pelser, P., du, T., 1977. Postharvest handling of South African citrus fruit. Proc. Int. Soc. Citriculture 1: 244–249.
  28. Pérez, E., Blanco, O., Berreta, C., Dol, I., Lado, J., 2011. Imazalil concentration for in vitro monitoring of imazalil resistant isolates of Penicillium digitatumin citrus packinghouses. Postharvest Biology and Technology 60, 258–262.
  29. Pitt, J. I., & Hocking, A. D. (2009). Fungi and food spoilage (Vol. 519, p. 388). New York: Springer.
  30. Ramirez, C. 1982. Manual and Atlas of the Penicillia. Elsevier Biomedical Press, Amsterdam, 482 pp.
  31. Sánchez-Torres, P., Tuset, J., 2011. Molecular insights into fungicide resistance in sensitive and resistant Penicillium digitatumstrains infecting citrus. Postharvest Biology and Technology59: 159–165.
  32. Samson, R. A., Hoekstra, E. S., & Frisvad, J. C. (2004). Introduction to food-and airborne fungi (No. Ed. 7). Centraalbureau voor Schimmelcultures (CBS).
  33. Sholberg, P. L., Bedford, K., and Stokes, S. 2005. Sensitivity of Penicillium spp. and Botrytis cinerea to pyrimethanil and its control of blue and gray mold of stored apples. CropProtection 24:127-134.
  34. Smilanick, J. L., Mansour, M. F., Mlikota Gabler, F., and Goodwine, W. R. Erasmus, A., Lennox. 2006 The effectiveness of pyrimethanil to inhibit germination of Penicillium digitatum and to control citrus green mold after harvest. Postharvest Biology and Technology42:75-85.
  35. Smilanick, J.L., Mansour, M.F., Gabler, F.M., Sorenson, D., 2008. Control of citrus postharvest green mold and sour rot by potassium sorbate combined with heat and fungicides. Postharvest Biology and Technology 47: 226–238
  36. Smilanick, J.L., Mansour, M.F., Mlikota-Gabler, F., andGoodwine, W.R. 2006. The effectiveness of pyrimethanil to inhibit germination of Penicillium digitatumand to control citrus green mold after harvest. Postharvest Biology and Technology 42: 75–85.
  37. Tuset, J. J. (1987). Podredumbres de los frutos cítricos. Conselleria d'Agricultura i Pesca/IVIA.
  38. Wild, B.L. 1994. Differential sensitivity of citrus green mould isolates (Penicillium digitatumSacc.) to the fungicide imazalil. New Zealand Journal of Crop and Horticultural Science 22: 167–171.
  39. Wolfe, M. S. (1982). Dynamics of the pathogen population in relation to fungicide resistance. Fungicide resistance in crop protection, 139-148.
  40. Zhang, Z., Zhu, Z., andMa, Z., Li, H. 2009. Molecular mechanism of azoxystrobin resistance in Penicillium digitatumUV mutants and a PCR-based assay for detection of azoxystrobin-resistant strains in packing- or store-house isolates. Int. J. Food Microbiol. 131, 157–161.
  41. Zhu, J. W., Xie, Q. Y., and Li, H. Y. 2006. Occurrence of imazalil-resistant biotype of Penicillium digitatum in China and the resistant molecular mechanism. Journal of Zhejiang University-Science 7(Suppl 2): 362-365.