Effect of marine yeasts and ulvan on the postharvest control of Penicillium italicum causal agent of blue mold in Persian lemon
DOI:
https://doi.org/10.18633/biotecnia.v23i3.1428Keywords:
antagonistic mechanisms, biological control, fruits, defense enzymesAbstract
Penicillium italicum is causing blue mold on citrus fruits. Its control is with synthetic fungicides, however, marine yeasts and ulvan are an alternative to synthetic agro-products. The objective of this study was to determine in vitro antagonism of yeasts against P. italicum and its effect with ulvan in the control of blue mold in Persian lemon fruits. The effect of ulvan on P. italicum and yeasts was evaluated. In vitro antagonism was determined by confrontation between yeast-phytopathogen and competition for carbohydrates. The protection of fruits with yeasts and ulvan against P. italicum was evaluated and the severity and incidence of the disease and the expression of SOD, POX and CAT were determined. There was no effect of ulvan on microorganisms. In vitro, yeasts inhibited the phytopathogen. Carbohydrates decreased with yeast and P. italicum, and spore germination of the phytopathogen was inhibited. The incidence of P. italicum in the fruits was decreased by yeast and ulvan. POX, CAT and SOD were increased in the fruits with yeast and ulvan. The application of marine yeasts and ulvan may be an option in the control of blue mold in Persian lemon fruits.
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References
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Chen, C., Wan, C., Peng, X., Chen, J. 2020. A flavonone pinocembroside inhibits Penicillium italicum growth and blue mold development in ‘Newhall’ navel oranges by targeting membrane damage mechanism. Pesticide Biochemistry and Physiology. 165, 104505.
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Czarnecka, M., Żarowska, B., Połomska, X., Restuccia, C., Cirvilleri, G. 2019. Role of biocontrol yeasts Debaryomyces hansenii and Wickerhamomyces anomalus in plants defence mechanisms against Monilinia fructicola in apple fruits. Food Microbiology. 83, 1-8.
Droby, S., Wisniewski, M., Macarisin, D., Wilson, C. 2009. Twenty years of postharvest biocontrol research: is it time for a new paradigma?. Postharvest Biol. Technol. 52(2): 137-145.
El-Otmani, M., Ait-Oubahou, A., Zacarías, L. 2011. Citrus spp.: orange, mandarin, tangerine, clementine, grapefruit, pomelo, lemon and lime. In: Postharvest biology and technology of tropical and subtropical fruits (pp. 437-516e). Woodhead Publishing.
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Jain, A., Chatterjee, A., Das, S. 2020. Synergistic consortium of beneficial microorganisms in rice rhizosphere promotes host defense to blight-causing Xanthomonas oryzae pv. oryzae. Planta. 252(6): 1-25.
Jing, J., Zhang, H., Xue, Y., Zeng, K. 2020. Effects of INA on postharvest blue and green molds and anthracnose decay in citrus fruit. Journal of Integrative Agriculture. 19(5): 1396-1406.
Kanashiro, A., Akiyama, D., Kupper, K., Fill, T. 2020. Penicillium italicum: an underexplored postharvest pathogen. Frontiers in Microbiology. 11.
Kellerman, M., Joubert, J., Erasmus, A., Fourie, P. 2016. The effect of temperature, exposure time and pH on imazalil residue loading and green mould control on citrus through dip application. Postharvest Biology and Technology. 121, 159-164.
Khedia, J., Dangariya, M., Nakum, A., Agarwal, P., Panda, A., Parida, A., Gangapur, D., Meena, R., Agarwal, P. 2020. Sargassum seaweed extract enhances Macrophomina phaseolina resistance in tomato by regulating phytohormones and antioxidative activity. Journal of Applied Phycology. 32(6): 4373-4384.
Klein, A., Hüsselmann, L., Keyster, M., Ludidi, N. 2018. Exogenous nitric oxide limits salt-induced oxidative damage in maize by altering superoxide dismutase activity. South African Journal of Botany. 115, 44-49.
Konsue, W., Dethoup, T., Limtong, S. 2020. Biological control of fruit rot and anthracnose of postharvest mango by antagonistic yeasts from economic crops leaves. Microorganisms. 8(3), 317.
Li, B., Xu, H., Wang, X., Wan, Y., Jiang, N., Qi, H., Liu, X. 2020. Antioxidant and antihyperlipidemic activities of high sulfate content purified polysaccharide from Ulva pertusa. International Journal of Biological Macromolecules. 146, 756-762.
Moenne, A., Gómez, M., Laporte, D., Espinoza, D., Sáez, C., González, A. 2020. Mechanisms of copper tolerance, accumulation, and detoxification in the marine macroalga Ulva compressa (Chlorophyta): 20 years of research. Plants. 9(6): 681.
Moussa, H., El Omari, B., Chefchaou, H., Tanghort, M., Mzabi, A., Chami, N., Remmal, A. 2020. Action of thymol, carvacrol and eugenol on Penicillium and Geotrichum isolates resistant to commercial fungicides and causing postharvest citrus decay. Canadian Journal of Plant Pathology. 1-9.
Mukherjee, A., Verma, J., Gaurav, A., Chouhan, G., Patel, J.., Hesham, A. 2020. Yeast a potential bio-agent: future for plant growth and postharvest disease management for sustainable agriculture. Applied Microbiology and Biotechnology. 104(4): 1497-1510.
Ochoa, J., Hernandez-Montiel, L., Latisnere-Barragan, H., León de la Luz, J., Larralde-Corona, C. 2007. Aislamiento e identificación de hongos patógenos de naranja (Citrus sinensis L. Osbeck) cultivada en Baja California Sur, México. Ciencia y Tecnología Alimentaria. 5, 352-359.
Ons, L., Bylemans, D., Thevissen, K., Cammue, B. 2020. Combining biocontrol agents with chemical fungicides for integrated plant fungal disease control. Microorganisms. 8(12): 1930.
Palmieri, D., Vitullo, D., De Curtis, F., Lima, G. 2017. A microbial consortium in the rhizosphere as a new biocontrol approach against fusarium decline of chickpea. Plant and Soil. 412(1-2): 425-439.
Pandhal, J., Noirel, J. 2014. Synthetic microbial ecosystems for biotechnology. Biotechnol. Lett. 36, 1141-1151.
Panebianco, S., Vitale, A., Polizzi, G., Scala, F., Cirivilleri, G. 2015. Enhanced control of postharvest citrus fruit decay bymeans of the combined use of compatible biocontrol agents. Biological Control. 84, 19-27.
Pankiewicz, R., Leska, B., Messyasz, B., Fabrowska, J., Soloducha, M., Pikosz, M. 2016. First isolation of polysaccharides ulvans from the cell walls of freshwater algae. Algal Research. 19, 348-35.
Papoutsis, K., Mathioudakis, M., Hasperué, J., Ziogas, V. 2019. Non-chemical treatments for preventing the postharvest fungal rotting of citrus caused by Penicillium digitatum (green mold) and Penicillium italicum (blue mold). Trends in Food Science and Technology. 86, 479-491.
Qi, C., Lin, X., Li, S., Liu, L., Wang, Z., Li, Y., Bai, R., Xie, Q., Zhang, N., Ren, S., Zhao, B., Li, X., Fan, S., Guo, Y. 2019. SoHSC70 positively regulates thermotolerance by alleviating cell membrane damage, reducing ROS accumulation, and improving activities of antioxidant enzymes. Plant Science. 283, 385-395.
Rivas-Garcia, T., Murillo-Amador, B., Nieto-Garibay, A., Chiquito-Contreras, R., Rincon-Enriquez, G., Hernandez-Montiel, L. 2018. Effect of ulvan on the biocontrol activity of Debaryomyces hansenii and Stenotrophomonas rhizophila against fruit rot of Cucumis melo L. Agronomy. 8(12); 273.
SADER, 2019. Estadísticas de cítricos, Superficie Cosechada, Sembrada y Producción. www.gob.mx
Solairaj, D., Legrand, N., Yang, Q., Zhang, H. 2020. Isolation of pathogenic fungi causing postharvest decay in table graps and in vivo biocontrol activity of selected yeasts against them. Physiological and Molecular Plant Pathology. 110, 101478.
Spadaro, D., Ciavorella, A., Dianpeng, Z., Garibaldi, A., Gullino, M. 2010. Effect of culture media and pH on the biomass production and biocontrol efficacy of a Metschnikowia pulcherrima strain to be used as a biofungicide for postharvest disease control. Canadian Journal of Microbiology. 56(2); 128-137.
Spadaro, D., Droby, S. 2016. Development of biocontrol products for postharvest diseases of fruit: the importance of elucidating the mechanisms of action of yeast antagonists. Trends Food. Sci. Technol. 47: 39-49.
Sui, Y., Wisniewski, M., Droby, S., Piombo, E., Wu, X., Yue, J. 2020. Genome sequence, assembly, and characterization of the antagonistic yeast Candida oleophila used as a biocontrol agent against post-harvest diseases. Frontiers in Microbiology. 11, 295.
Taqarort, N., Echairi, A., Chaussod, R., Nouaim, R., Boubaker, H., Benaoumar, A., Boudyach, E. 2008. Screening and identification of epiphytic yeasts with potential for biological control of green mold of citrus fruits. World Journal of Microbiology and Biotechnology. 24, 3031-3038.
Wassermann, B., Kusstatscher, P., Berg, G. 2019. Microbiome response to hot water treatment and potential synergy with biological control on stored apples. Frontiers in Microbiology. 10, 2502.
Zhang, H., Zheng, X., Yu, T. 2007. Biological control of postharvest diseases of peach with Cryptococcus laurentii. Food Control. 18(4): 287-291.
Zhang, X., Zong, Y., Li, Z., Yang, R., Li, Z., Bi, Y., Prusky, D. 2020. Postharvest Pichia guilliermondii treatment promotes wound healing of apple fruits. Postharvest Biology and Technology. 167, 111228.
Zhimo, V. Y., Biasi, A., Kumar, A., Feygenberg, O., Salim, S., Vero, S., Wisniewski, M., Droby, S. 2020. Yeasts and bacterial consortia from kefir grains are effective biocontrol agents of postharvest diseases of fruits. Microorganisms. 8(3): 428.
Zhu, J., Gao, J., Yang, C., Shang, X., Zhao, Z., Lawoe, R., Zhou, R., Sun, Y., Yin, X., Liu, Y. 2020. Design, synthesis, and antifungal evaluation of neocryptolepine derivatives against phytopathogenic fungi. Journal of Agricultural and Food Chemistry. 68(8): 2306-2315.
Adrees, H., Haider, M., Anjum, T., Akram, W. 2019. Inducing systemic resistance in cotton plants against charcoal root rot pathogen using indigenous rhizospheric bacterial strains and chemical elicitors. Crop Prot. 115. 75-83
Berri, M., Slugocki, C., Oliver, M., Helloin, E., Jacques, I., Salmon, H., Le Goff, M., Collen, P. 2016. Marine sulfated polysaccharides extract of Ulva armoricana green algae exhibits an antimicrobial activity and stimulates cytokine expression by intestinal epithelial cell. Journal Applied Phycol. 28, 2999-3008.
Chen, C., Wan, C., Peng, X., Chen, J. 2020. A flavonone pinocembroside inhibits Penicillium italicum growth and blue mold development in ‘Newhall’ navel oranges by targeting membrane damage mechanism. Pesticide Biochemistry and Physiology. 165, 104505.
Chiquito-Contreras, R., Murillo-Amador, B., Carmona-Hernandez, S., Chiquito-Contreras, C., Hernandez-Montiel, L. 2019. Effect of marine bacteria and ulvan on the activity of antioxidant defense enzymes and the bio-protection of papaya fruit against Colletotrichum gloeosporioides. Antioxidants. 8(12): 580.
Czarnecka, M., Żarowska, B., Połomska, X., Restuccia, C., Cirvilleri, G. 2019. Role of biocontrol yeasts Debaryomyces hansenii and Wickerhamomyces anomalus in plants defence mechanisms against Monilinia fructicola in apple fruits. Food Microbiology. 83, 1-8.
Droby, S., Wisniewski, M., Macarisin, D., Wilson, C. 2009. Twenty years of postharvest biocontrol research: is it time for a new paradigma?. Postharvest Biol. Technol. 52(2): 137-145.
El-Otmani, M., Ait-Oubahou, A., Zacarías, L. 2011. Citrus spp.: orange, mandarin, tangerine, clementine, grapefruit, pomelo, lemon and lime. In: Postharvest biology and technology of tropical and subtropical fruits (pp. 437-516e). Woodhead Publishing.
FAO. 2019. Annual statistics. http://www.fao.
Guo, K., Li, Z., Tian, H., Du, X., Liu, Z., Huang, H., Wang, P., Ye, Z., Zhang, X., Tu, L. 2020. Cytosolic ascorbate peroxidases plays a critical role in photosynthesis by modulating reactive oxygen species level in stomatal guard Cell. Frontiers in Plant Science. 11, 446.
Hernandez-Montiel, L., Ochoa, J., Troyo-Diéguez, E., Larralde-Corona, C. 2010. Biocontrol of postharvest blue mold (Penicillium italicum Wehmer) on Mexican lime by marine and citrus Debaryomyces hansenii isolates. Postharvest Biol. Technol. 56(2): 181-187.
Jain, A., Chatterjee, A., Das, S. 2020. Synergistic consortium of beneficial microorganisms in rice rhizosphere promotes host defense to blight-causing Xanthomonas oryzae pv. oryzae. Planta. 252(6): 1-25.
Jing, J., Zhang, H., Xue, Y., Zeng, K. 2020. Effects of INA on postharvest blue and green molds and anthracnose decay in citrus fruit. Journal of Integrative Agriculture. 19(5): 1396-1406.
Kanashiro, A., Akiyama, D., Kupper, K., Fill, T. 2020. Penicillium italicum: an underexplored postharvest pathogen. Frontiers in Microbiology. 11.
Kellerman, M., Joubert, J., Erasmus, A., Fourie, P. 2016. The effect of temperature, exposure time and pH on imazalil residue loading and green mould control on citrus through dip application. Postharvest Biology and Technology. 121, 159-164.
Khedia, J., Dangariya, M., Nakum, A., Agarwal, P., Panda, A., Parida, A., Gangapur, D., Meena, R., Agarwal, P. 2020. Sargassum seaweed extract enhances Macrophomina phaseolina resistance in tomato by regulating phytohormones and antioxidative activity. Journal of Applied Phycology. 32(6): 4373-4384.
Klein, A., Hüsselmann, L., Keyster, M., Ludidi, N. 2018. Exogenous nitric oxide limits salt-induced oxidative damage in maize by altering superoxide dismutase activity. South African Journal of Botany. 115, 44-49.
Konsue, W., Dethoup, T., Limtong, S. 2020. Biological control of fruit rot and anthracnose of postharvest mango by antagonistic yeasts from economic crops leaves. Microorganisms. 8(3), 317.
Li, B., Xu, H., Wang, X., Wan, Y., Jiang, N., Qi, H., Liu, X. 2020. Antioxidant and antihyperlipidemic activities of high sulfate content purified polysaccharide from Ulva pertusa. International Journal of Biological Macromolecules. 146, 756-762.
Moenne, A., Gómez, M., Laporte, D., Espinoza, D., Sáez, C., González, A. 2020. Mechanisms of copper tolerance, accumulation, and detoxification in the marine macroalga Ulva compressa (Chlorophyta): 20 years of research. Plants. 9(6): 681.
Moussa, H., El Omari, B., Chefchaou, H., Tanghort, M., Mzabi, A., Chami, N., Remmal, A. 2020. Action of thymol, carvacrol and eugenol on Penicillium and Geotrichum isolates resistant to commercial fungicides and causing postharvest citrus decay. Canadian Journal of Plant Pathology. 1-9.
Mukherjee, A., Verma, J., Gaurav, A., Chouhan, G., Patel, J.., Hesham, A. 2020. Yeast a potential bio-agent: future for plant growth and postharvest disease management for sustainable agriculture. Applied Microbiology and Biotechnology. 104(4): 1497-1510.
Ochoa, J., Hernandez-Montiel, L., Latisnere-Barragan, H., León de la Luz, J., Larralde-Corona, C. 2007. Aislamiento e identificación de hongos patógenos de naranja (Citrus sinensis L. Osbeck) cultivada en Baja California Sur, México. Ciencia y Tecnología Alimentaria. 5, 352-359.
Ons, L., Bylemans, D., Thevissen, K., Cammue, B. 2020. Combining biocontrol agents with chemical fungicides for integrated plant fungal disease control. Microorganisms. 8(12): 1930.
Palmieri, D., Vitullo, D., De Curtis, F., Lima, G. 2017. A microbial consortium in the rhizosphere as a new biocontrol approach against fusarium decline of chickpea. Plant and Soil. 412(1-2): 425-439.
Pandhal, J., Noirel, J. 2014. Synthetic microbial ecosystems for biotechnology. Biotechnol. Lett. 36, 1141-1151.
Panebianco, S., Vitale, A., Polizzi, G., Scala, F., Cirivilleri, G. 2015. Enhanced control of postharvest citrus fruit decay bymeans of the combined use of compatible biocontrol agents. Biological Control. 84, 19-27.
Pankiewicz, R., Leska, B., Messyasz, B., Fabrowska, J., Soloducha, M., Pikosz, M. 2016. First isolation of polysaccharides ulvans from the cell walls of freshwater algae. Algal Research. 19, 348-35.
Papoutsis, K., Mathioudakis, M., Hasperué, J., Ziogas, V. 2019. Non-chemical treatments for preventing the postharvest fungal rotting of citrus caused by Penicillium digitatum (green mold) and Penicillium italicum (blue mold). Trends in Food Science and Technology. 86, 479-491.
Qi, C., Lin, X., Li, S., Liu, L., Wang, Z., Li, Y., Bai, R., Xie, Q., Zhang, N., Ren, S., Zhao, B., Li, X., Fan, S., Guo, Y. 2019. SoHSC70 positively regulates thermotolerance by alleviating cell membrane damage, reducing ROS accumulation, and improving activities of antioxidant enzymes. Plant Science. 283, 385-395.
Rivas-Garcia, T., Murillo-Amador, B., Nieto-Garibay, A., Chiquito-Contreras, R., Rincon-Enriquez, G., Hernandez-Montiel, L. 2018. Effect of ulvan on the biocontrol activity of Debaryomyces hansenii and Stenotrophomonas rhizophila against fruit rot of Cucumis melo L. Agronomy. 8(12); 273.
SADER, 2019. Estadísticas de cítricos, Superficie Cosechada, Sembrada y Producción. www.gob.mx
Solairaj, D., Legrand, N., Yang, Q., Zhang, H. 2020. Isolation of pathogenic fungi causing postharvest decay in table graps and in vivo biocontrol activity of selected yeasts against them. Physiological and Molecular Plant Pathology. 110, 101478.
Spadaro, D., Ciavorella, A., Dianpeng, Z., Garibaldi, A., Gullino, M. 2010. Effect of culture media and pH on the biomass production and biocontrol efficacy of a Metschnikowia pulcherrima strain to be used as a biofungicide for postharvest disease control. Canadian Journal of Microbiology. 56(2); 128-137.
Spadaro, D., Droby, S. 2016. Development of biocontrol products for postharvest diseases of fruit: the importance of elucidating the mechanisms of action of yeast antagonists. Trends Food. Sci. Technol. 47: 39-49.
Sui, Y., Wisniewski, M., Droby, S., Piombo, E., Wu, X., Yue, J. 2020. Genome sequence, assembly, and characterization of the antagonistic yeast Candida oleophila used as a biocontrol agent against post-harvest diseases. Frontiers in Microbiology. 11, 295.
Taqarort, N., Echairi, A., Chaussod, R., Nouaim, R., Boubaker, H., Benaoumar, A., Boudyach, E. 2008. Screening and identification of epiphytic yeasts with potential for biological control of green mold of citrus fruits. World Journal of Microbiology and Biotechnology. 24, 3031-3038.
Wassermann, B., Kusstatscher, P., Berg, G. 2019. Microbiome response to hot water treatment and potential synergy with biological control on stored apples. Frontiers in Microbiology. 10, 2502.
Zhang, H., Zheng, X., Yu, T. 2007. Biological control of postharvest diseases of peach with Cryptococcus laurentii. Food Control. 18(4): 287-291.
Zhang, X., Zong, Y., Li, Z., Yang, R., Li, Z., Bi, Y., Prusky, D. 2020. Postharvest Pichia guilliermondii treatment promotes wound healing of apple fruits. Postharvest Biology and Technology. 167, 111228.
Zhimo, V. Y., Biasi, A., Kumar, A., Feygenberg, O., Salim, S., Vero, S., Wisniewski, M., Droby, S. 2020. Yeasts and bacterial consortia from kefir grains are effective biocontrol agents of postharvest diseases of fruits. Microorganisms. 8(3): 428.
Zhu, J., Gao, J., Yang, C., Shang, X., Zhao, Z., Lawoe, R., Zhou, R., Sun, Y., Yin, X., Liu, Y. 2020. Design, synthesis, and antifungal evaluation of neocryptolepine derivatives against phytopathogenic fungi. Journal of Agricultural and Food Chemistry. 68(8): 2306-2315.
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2021-09-29
How to Cite
Vázquez-Vázquez, M. L., Chiquito-Contreras, R., Sanchez-Viveros, G., Reyes-Pérez, J., Martinez-Hernandez, M., & Hernández Montiel, L. G. (2021). Effect of marine yeasts and ulvan on the postharvest control of Penicillium italicum causal agent of blue mold in Persian lemon. Biotecnia, 23(3), 78–88. https://doi.org/10.18633/biotecnia.v23i3.1428
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