Biological control of citrus blast disease using some yeast strains isolated from citrus orchards in the northern provinces of Iran

Document Type : Research Paper

Authors

Abstract

Citrus blast caused by Pseudomonas spp. is one of the most important diseases in the northern citrus growing provinces of Iran which causes considerable losses to citrus orchards in conducive climatic conditions. In this study, we tried to isolate and introduce some yeast strains from citrus orchards with acceptable biological control potential against the disease. The evaluations were performed under green house conditions on sour orange seedlings. Yeast cell suspensions were sprayed three times with two-days intervals on seedlings before pathogen inoculation. Statistical analysis of the results was carried out using Randomized Complete Block experimental design and comparison of disease severity means was performed by Duncan's Multiple Range Test. For the identification of the effective yeast strains, ITS regions of their rRNA operon were amplified using universal primers (ITS1 and ITS4) by PCR and the amplified fragments were sequenced. Based on the above procedures and comparison of the sequences with those deposited in the GenBank, the effective yeasts were identified as Sporobolomyces ruberrimus, Cryptococcus albidus, C. magnus and Rhodotorula sp.According to the results, S. ruberrimus, was the most effective yeast and controlled the disease more efficiently than other species.

Keywords


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: 191-198.
Arras, G., Cicco, V., Arru, S. & Lima, G. 1998. Biocontrol by yeasts of blue mould of citrus fruits and the mode of action of an isolate of Pichia guilliermondii. Journal of Horticultural Science and Biotechnology. 73: 413-418.
Bar-Shimon, M., Yehuda, H., Cohen, L., Weiss, B., Kobeshnikov, A., Daus, A., Goldway, M., Wisniewski, M. & Droby, S. 2004. Characterization of extracellular lytic enzymes produced by the yeast biocontrol agent Candida oleophila. Current Genetics. 45: 140-148.
Barkai-Golan, R. 2001. Postharvest Diseases of Fruits and Vegetables: Development and Control. Elsevier Science, Amsterdam.
Basse, C. W. & Boller, T. 1992. Glycopeptide elicitors of stress responses in tomato cells: N-linked glycans are essential for activity but act as suppressors of the same activity when released from the glycopeptides. Plant Physiology. 98: 1239-1247.
Benbow, J. M. & Sugar, D. 1999. Fruit surface colonization and biological control of postharvest diseases of pear by preharvest yeast applications. Plant Disease. 83: 839-844.
Calvo, J., Calvente, V., De Orellano, M. E., Benuzzi, D. & De Tosetti, M. I. S. 2003. Improvement in the biocontrol of postharvest diseases of apples with the use of yeast mixtures. Biocontrol. 48: 579-593.
Cao, H., Baldini, R. L. & Rahme, L. G. 2001. Common mechanisms for pathogens of plants and animals. Annual Review of Phytopathology. 39: 259-284.
Castoria, R., Morena, V., Caputo, L., Panfili, G., De Curtis, F. & De Cicco, V. 2005. Effect of the biocontrol yeast Rhodotorula glutinis strain LS11 on patulin accumulation in stored apples. Phytopathology. 95: 1271-1278.
Chalutz, E. & Wilson, C. L. 1990. Postharvest biocontrol of green and blue mold and sour rot of citrus fruit by Debaryomyces hansenii. Plant Disease. 74: 134-137.
Chalutz, E., Ben-Arie, R., Droby, S., Cohen, L., Weiss, B. & Wilson, C. L. 1988. Yeasts as biocontrol agents of postharvest diseases of fruits. Phytoparasitica. 16: 69-75.
Chan, Z. L., Qin, G. Z., Xu, X. B., Li, B. Q. & Tian, S. P. 2007. Proteome approach to characterize proteins induced by antagonist yeast and salicylic acid in peach fruit. Journal of Proteome Research. 6: 1677-1688.
Chandgoyal, T. & Spotts, R. A. 1996. Control of postharvest pear diseases using natural saprophytic yeast colonists and their combination with a low dosage of thiabendazole. Postharvest Biology and Technology. 7: 51-64.
Dangl, J. L. & Jones, J. D. G. 2001. Plant pathogens and integrated defence responses to infection. Nature. 411: 826-833.
De Capdeville, G., Wilson, C. L., Beer, S. V. & Aist, J. R. 2002. Alternative disease control agents induce resistance to blue mold in harvested 'Red Delicious' apple fruit. Phytopathology. 92: 900-908.
De Capdeville, G., Souza, M. T., Santos, J. R. P., Miranda, S. P., Caetano, A. R. & Torres, F.  A. G. 2007. Selection and testing of epiphytic yeasts to control anthacnose in post-harvest of papaya fruit. Scientia Horticulturae. 111: 179-185.
Droby, S. & Chalutz, E. 1994. Mode of action of biocontrol agents of postharvest diseases. pp. 63-75. In:Wilson, C. L. & Wisniewski, M. E. (eds.),Biological Control of Postharvest Diseases of Fruits and Vegetables-Theory and Practice, CRC Press, Boca Raton.
Droby, S., Chalutz, E., Wilson, C. L & Wisniewski, M. 1989. Characterization of the biocontrol activity of Debaryomyces hansenii in the control of Penicillium digitatum on grapefruit. Canadian Journal of Microbiology. 35: 794-800.
Droby, S., Chalutz, E., Wilson, C. L. & Wisniewski, M. E. 1992. Biological control of postharvest diseases: A promising alternative to the use of synthetic fungicides. Phytoparasitica. 20: 149-153.
Droby, S., Porat, R., Vinokur, V., Cohen, L., Weiss, B. & Daus, A. 2000. Induction of resistance to postharvest decay by the yeast biocontrol agent Candida oleophila. Photopathology. 24: 297-301.
El-Ghaouth, A. 1997. Biologically-based alternatives to synthetic fungicides for the control of postharvest diseases. Journal of Industrial Microbiology & Biotechnology. 19: 160-162.
El-Ghaouth, A., Wilson, C. L. & Wisniewski, M. 1998. Ultrastructural and cytochemical aspects of the biological control of Botrytis cinerea by Candida saitoana in apple fruit. Phytopathology. 88: 282-291.
El-Ghaouth, A., Wilson, C. & Wisniewski, M. 2001. Induction of systemic resistance in apple by the yeast antagonist Candida saitoana. Bulletin OILB/SROP. 24: 309-312.
El-Ghaouth, A., Smilanick, J. L., Brown, G. E., Ippolito, A., Wisniewski, M. & Wilson, C. L. 2000. Application of Candida saitoana and glycolchitosan for the control of postharvest diseases of apple and citrus fruit under semi-commercial conditions. Plant Disease. 84: 243-248.
El-Neshawy, S. M. & El-Sheikh, M. M. 1998. Control of green mold on oranges by Candida oleophila and calcium treatments. Annals of Agricultural Sciences Cairo. 3: 881-890.
Elmer, P. A. G. & Reglinski, T. 2006. Biosuppression of Botrytis cinerea in grapes. Plant Pathology. 55: 155-177.
Esteve-Zarzoso, B., Belloch, C., Uruburu, F. & Querol, A. 1999. Identification of yeasts by RFLP analysis of the 5.8S rRNA gene and the two ribosomal internal transcribed spacers. International Journal of Systematic Bacteriology. 49: 329-337.
Fajardo, J., McCollum, T., McDonald, R. & Mayer, R. 1998. Differential induction of proteins in orange flavedo by biologically based elicitors and challenged by Penicillium digitatum. Biological Control. 13: 143-151.
Filonow, A., Vishniac, H., Anderson, J. & Janisiewicz, W. 1996. Biological control of Botrytis cinereain apple by yeasts from various habitats and their putative mechanisms of antagonism. Biological Control. 7: 212-220.
Ghasemi, S., Etebarian, H., Sahebani, N. & Aminian, H. 2011. Control of blue mold on orange fruit by yeast, Metschnikowia pulcherrima (m54) and induction of b 1,3-glucanase enzyme in albedo and flavedo tissues.Proceeding of the biological control development congress in Iran, 27-28 July, Tehran, Iran, 477. (In Persian with English summary)
Gholamnejad, J., Etebarian, H. R. & Sahebani, N. 2010. Biological control of apple blue mold with Candida membranifaciens and Rhodotorula mucilaginosa. African Journal of Food Science. 4: 1-7.
Gholamnejad, J., Etebarian, H. R., Roustaee, A. & Sahebani, N. A. 2009. Biological control of apples blue mold by isolates of Saccharomyces cerevisiae. Journal of Plant Protection Research. 49: 270-275. (In Persian with English summary)
Gnanamanickam, S. S. 2007. Plant Aassociated Bacteria. Springer, Dordrecht.
Hashem, M. & Alamri, S. 2009. The biocontrol of postharvest disease (Botryodiplodia theobromae) of guava (Psidium guajava L.) by the application of yeast strains. Postharvest Biology and Technology. 53: 123-130.
Hwang, M. S. H., Morgan, R. L., Sarkar, S. F., Wang, P. W. & Guttman, D. S. 2005. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Applied and Environmental Microbiology. 71: 5182-5191.
Ippolito, A. & Nigro, F. 2000. Impact of preharvest application of biological control agents on postharvest diseases of fresh fruits and vegetables. Crop Protection. 19: 715,723.
Janisiewicz, W. J. 1987. Postharvest biological control of blue mold on apples. Phytopathology. 77: 481-485.
Karabulut, O. A. & Baykal, N. 2003. Biological control of postharvest diseases of peaches and nectarines by yeasts. Journal of Phytopathology. 151: 130-134.
Klotz, L. J. 1978. Fungal, bacterial, and non parasitic diseases and injuries originating in the seedbed, nursery, and orchard. pp. 1-23. In: Reuther, W., Calavan, E. C. & Carman, G. E. (eds.), The Citrus Industry: IV. Crop Protection, University of California Press, Berkely.
Kurtzman, C. P. & Fell, J. W. 1998. The Yeasts, a Txonomic Study. Elsevier Science, Amesterdam.
Lahlali, R., Serrhini, M. & Jijakli, M. 2004. Efficacy assessment of Candida oleophila (strain O) and Pichia anomala (strain K) against major postharvest diseases of citrus fruits in Morocco. Communications in Agricultural and Applied Biological Sciences. 69: 601-609.
Liu, X., Fang, W., Liu, L., Yu, T., Lou, B. & Zheng, X. 2010. Biological control of postharvest sour rot of citrus by two antagonistic yeasts. Letters in Applied Microbiology. 51: 30-35.
Long, C., Deng, B. & Deng, X. 2007. Commercial testing of Kloeckera apiculata, isolate 34-9, for biological control of postharvest diseases of citrus fruit. Annals of Microbiology. 57: 203-207.
Mercier, J. & Wilson, C. L. 1994. Colonization of apple wounds by naturally occurring microflora and introduced Candida oleophila and their effect on infection by Botrytis cinerea during storage. Biological Control. 4: 138-144.
Nurnberger, T., Brunner, F., Kemmerling, B. & Piater, L. 2004. Innate immunity in plants and animals: Striking similarities and obvious differences. Immunological Reviews. 198: 249-266.
Porat, R., Vinocur, V., Weiss, B., Cohen, L. & Droby, S. 1999. Effects of various elicitors on the resistance of citrus fruit against pathogens. Phytoparasitica. 27: 157-158.
Raacke, I., Von Rad, U., Mueller, M. & Berger, S. 2006. Yeast increases resistance in Arabidopsis against Pseudomonas syringae and Botrytis cinerea by salicylic acid-dependent as well as independent mechanisms. Molecular Plant-Microbe Interactions. 19: 1138-1146.
Seyfi, R., Nahvi, I. & Balali, G. 2006. Investigation of biological control of post harvest diseases on apple by yeast Metschenikowia pulcherrima. Iranian Journal of Biology. 19: 64-76. (In Persian with English summary)
Shams-Bakhsh, M. & Rahimian, H. 1997. Comparative study on agents of citrus blast and bacterial canker of stone fruits in Mazandaran. Iranian Journal of Plant Pathology. 33: 132-143. (In Persian with English summary)
Sharma, R. R., Dinesh, S. & Rajbir, S. 2009. Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: A review. Biological Control. 50: 205-221.
Shulaev, V., León, J. & Raskin, I. 1995. Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? The Plant Cell. 7: 1691-1701.
Snowdon, A. L. 1990. A Colour Atlas of Postharvest Diseases and Disorders of Fruits and Vegetables. Manson Publishing, London.
Suzuki, H., Reddy, M. S. S., Naoumkina, M., Aziz, N., May, G. D., Huhman, D. V., Sumner, L. W., Blount, J. W., Mendes, P. & Dixon, R. A. 2005. Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta. 220: 696-707.
Tian, S. P., Fan, Q., Xu, Y. & Liu, H. B. 2002. Biocontrol efficacy of antagonist yeasts to gray mold and blue mold on apples and pears in controlled atmospheres. Plant Disease. 86: 848-853.
Wang, X., Li, G., Jiang, D. & Huang, H. C. 2009. Screening of plant epiphytic yeasts for biocontrol of bacterial fruit blotch (Acidovorax avenae subsp. citrulli) of hami melon. Biological Control. 50: 164-171.
White, T. J., Bruns, T., Lee, S. & Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. pp. 315-322. In:Innis, M. A., Gelfand, D. H., Sninsky, J. J. & White, T. J. (eds.),PCR Protocols a Guide to Methods and Applications, Academic Press, San Diego.
Whiteside, J. O., Garnsey, S. M. & Timmer, L. W. 1989. Compendium of Citrus Diseases. American Phytopathology Society Press, Minnesota.
Wilson, C. L. & Chalutz, E. 1989. Postharvest biological control of Penicillium rots of citrus with antagonistic yeasts and bacteria. Scientia Horticulturae. 40: 105-112.
Wisniewski, M., Wilson, C. L., Chalutz, E. & Hershberger, W. 1988. Biological control of postharvest diseases of fruit: Inhibition of Botrytis rot on apple by an antagonistic yeast. 46th Annual meeting of the electron microscopy society of America, 7-12 August, San Francisco, U.S.A., 290-291.
Wisniewski, M., Biles, C., Droby, S., Mclaughlin, R., Wilson, C. & Chalutz, E. 1991. Mode of action of the postharvest biocontrol yeast, Pichia guilliermondii.1.Characterization of attachment to Botrytis cinerea. Physiological and Molecular Plant Pathology. 39: 245-258.
Zangouei, E., Etebarian, H. R. & Sahebani, N. A. 2010. Improving biocontrol of gray mold disease of apple using a mixture of yeast isolates. Iranian journal of plant protection science. 41: 361-372. (In Persian with English summary)
Zhang, L., Jiang, B., Mu, W. & Zhang, T. 2008. Characterization of d-tagatose 3-epimerase from Rhodobacter sphaeroides SK011. Journal of Biotechnology. 136: S726-S726.