Induced defense responses and control of blue mold of apple fruit by Zaatar (Zataria multiflora) extract
Subject Areas :
Food Science and Technology
Pedram Alimosazadeh
1
,
Syed javad Sanei
2
,
Abdol Hossein Taheri
3
1 - B.Sc. student, Department of Plant Protection, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
2 - Assistant professor, Department of Plant Protection, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
3 - Associate professor, Department of Plant Protection, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
Received: 2023-05-05
Accepted : 2023-08-17
Published : 2023-06-22
Keywords:
apple,
peroxidase,
Total phenol,
blue mold,
Shirazi thyme,
Abstract :
Blue mold, caused by Penicillium expansum, is considered one of the most serious postharvest diseases of apple fruits. This study was conducted to evaluate the efficacy of thyme methanol extract to control the postharvest blue mold of apple fruit and its possible modes of action through on induction of biochemical defense mechanisms. In this study, the effect of thyme methanol extract was tested on spore germination and colony growth in vitro and peroxidase activity and total phenolic in fruit tissue were evaluated by calorimetric assay. The results showed the inhibitory activity of thyme extract on P. expansum. The extract with 8-20 µg/ml concentrations had 17-33% and 24-36% inhibition of spore germination and colony growth diameter, respectively. Thyme extract decreased blue mold area by 23.63-61.20% and the most effective extract was at 13.88 mg/ml concentration. The relationship between time and thyme extract concentration in relation to decay area was described by the quadratic model. Fruits treated with thyme extract had significantly higher phenolic content and peroxidase activity than the control fruits. The highest content of phenolic compounds and peroxidase activity were achieved in the 6th and 9th days after inoculation. The results of the induction of resistance in this study suggest that the natural products used have the potential for use in the integrated management of blue mold.
References:
Amini, M., Safaie, N., Salmani, M.J. and Shams-Bakhsh, M. (2012). Antifungal activity of three medicinal plant essential oils against some phytopathogenic fungi. Trakia Journal of Sciences, 10: 1-8. [In Persian].
Bradford, M.M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry, 72: 248-254.
Cheng, H., Mou, Z., Wang, W., Zhang, W., Wang, Z. and Zhang, M. (2019). Chitosan-catechin coating as an antifungal and preservable agent for postharvest Satsuma oranges. Journal of Food Biochemistry, 43:e12779.
Cindi, M.D., Sivakumar, D., Romanazzi, G. and Soundy, P. (2016). Differential defense responses and brown rot control after essential oil fumigation in two Prunus persica cultivars during storage. Postharvest Biology and Technology, 19: 9-17.
De Capdeville, G., Beer, S.V., Wilson, C.L., and Aist, J.R. (2002). Alternative disease control agents induce resistance to blue mold in harvested red delicious apple fruit. Phytopathology. 92: 900-908.
Droby, S., Wsiniewski, M., Ei-Ghaouth, A. and Wilson, C. (2003). Biological control of postharvest diseases of fruits and vegetables: current achievements and future challenges. Acta Horticulture, 628: 703-713.
El-Ghaouth, A., Wilson, C.L. and Wisniewski, M. (2003). Control of postharvest decay of apple fruit with Candida saitoana and induction of defense responses. Phytopathology, 93: 344-348.
El-Ghaouth, A., Smilanick, J.L., Wisniewski, M. and Wilson, C.L. (2000). Improved control of apple and citrus fruit decay with a combination of Candida saitoana and 2-deoxy-D-glucose. Plant Disease, 84: 249-253.
Fajardo, J.E., McCollum, T.G., McDonald, R.E. and Mayer, R.T. (1998). Differential induction of proteins in orange Flavedo by biologically based elicitors and challenged by Penicillium digitatum Sacc. Biological Control, 13:143-151.
Gandomi Nasr-Abadi, H., Misaghi, A., Akhoundzadeh Basti, A. and Khosravi, A.R. (2008). Effects of Zataria multiflora Boiss essential oil on Aspergillus flavus. Journal of Medical Plants. 7: 45-451. [In Persian].
Gholamnejad, J. (2017). Effect of plant extracts against apple gray mold caused by Botrytis cinerea. Applied Microbiology in Food Industries, 3: 53-66.
Gholamnejad, J., Etebarian, H.R. and Sahebani N. (2010). Biological control of apple blue mold with Candida membranifaciens and Rhodotorula mucilaginosa. African Journal of Food Science, 4: 1-7.
Haider, S.A., Ahmad, S., Khan, A.S., Anjum, M.A., Nasir, M. and Naz, S. (2020). Effects of salicylic acid on postharvest fruit quality of “Kinnow” mandarin under cold storage. Scientia Horticulturae, 259: 108843.
Hasani, A., Jalili Marandi, R. and Ghosta, Y. (2009). Use of essential oils in control of grey mold (Botrytis cinerea) infection in of pear fruits. Iranian Journal of Horticultural Science 2009; 40: 85-94.
J.H., Ma, L.J., Wang, D.J., Zhang, M.Y. and Zhou, H.L. (2019). Ferulic acid treatment reinforces the resistance of postharvest apple fruit during gray mold infection. Journal of Plant Pathology, 101: 503-511.
Jiang, A.L., Tian, S.P. and Xu, Y. (2002). Effects of controlled atmosphere with high CO2 concentartions on post-harvest physiology and storability of napoleon sweet cherry. Acta Botanica Sinica, 44: 925-930.
Karimi, A. and Meiners, T. (2021). Antifungal activity of Zataria multiflora Boiss. Essential oils and changes in volatile compound composition under abiotic stress conditions, Industrial Crops and Products, 171: 113888.
Khosravi, A.R., Shokri, H., Sharifrohani, M., Ebrahimzadeh Mousavi, H. and Moosavi, Z. (2012). Evaluation of the antifungal activity of Zataria multiflora, Geranium herbarium, and Eucalyptus camaldolensis essential oils on Saprolegnia parasitica-infected rainbow trout (Oncorhynchus mykiss) eggs. Foodborne Pathogen Disease, 9: 674-679.
Li, S., Jiang, H., Wang, Y., Lyu, L., Prusky, D. and Ji, Y. (2020). Effect of benzothiadiazole treatment on improving the mitochondrial energy metabolism involved in induced resistance of apple fruit during postharvest storage. Food Chemistry, 302:125288.
Loncaric, A., Sarkanj, B., Gotal, A.M., Kovač, M., Nevistić, A., Fruk, G., Skendrović Babojelić, M., Babić, J., Miličević, B. and Kovač, T. (2021). Penicillium expansum Impact and patulin accumulation on conventional and traditional apple cultivars. Toxins (Basel), 4; 13(10):703.
Luciano-Rosario, D., Keller, N.P. and Jurick, W.M. (2020). Penicillium expansum: biology, omics, and management tools for a global postharvest pathogen causing blue mold of pome fruit. Molecular Plant Pathology, 21; 1391-1404.
Magri, A., Curci, M., Battaglia, V., Fiorentino, A. and Petriccione, M. (2023). Essential oils in postharvest treatment against microbial spoilage of the Rosaceae family fruits. Applied Chemistry, 3: 196-216.
Malencic, D., Popovic, M. and Miladinovic, J. (2007). Phenolic content and antioxidant properties of soybean (Glycine max (L.) Merr.) Seeds. Molecules, 12: 576-581.
Mohammadi-Pourfard, A., and Kavoosi, G. (2012). Chemical composition, radical scavenging, antibacterial and antifungal activities of Zataria multiflora Bioss essential oil and aqueous extract. Journal of Food Safety, 32: 326-32.
Naseri, M., Arouiee, H., Golmohammadzadeh, S., Jaafari, M.R. and Neamati, H. (2015). Antifungal effects of Zataria multiflora essential oil on the inhibitory growth of some postharvest pathogenic fungi. Notulae Scientia Biologicae, 7: 412-416.
Noori, N., Yahyaraeyat, R., Khosravi, A.R., Atefi, P., Akhondzadeh Basti, A., and Akrami, F. (2012). Effect of Zataria multiflora Bioss. Essential oil on growth and citrinin production by Penicillium citrinum in culture media and mozzarella cheese. Journal of Food Safety, 32: 445-451.
Ntasiou, P., Samaras, A., Karaoglanidis, G. (2021). Apple fruit core rot agents in Greece and control with succinate dehydrogenase inhibitor fungicides. Plant Disease, 105: 3072-3081.
Oroojalian, F., Kasra-Kermanshahi, R., Azizi, M. and Bassami, M.R. (2010). Phytochemical composition of the essential oils from three Apiaceae species and their antibacterial effects on food-borne pathogens. Food Chemistry, 120: 765-770.
Regnier, T., Combrinck, S., Veldman, W. and Duplooy, W. (2014). Application of essential oils as muti-target fungicides for the control of Geotrichum citri- aurantii and other postharvest pathogens of citrus. Industrial Crops and Products, 61: 151-159.
Sanderson, P.G. and Spotts, R.A. (1995). Postharvest decay of winter pear and apple fruit caused by species of Penicillium. Phytopathology, 85: 103-110.
Shokri, H. and Sharifzadeh, A. (2017). Zataria multiflora Boiss. A review study on chemical composition, antifungal and anti-mycotoxin activities, and ultrastructural changes. Journal of Herbmed Pharmacology, 6: 1-9.
Smith, K., SHewfeltoK, R.L., Maclcan, D.D. and Mehra, l.K. (2013). Effect of postharvest biofumigation on fungal decay, sensory quality, and antioxidant levels of blueberry fruit. Postharvest Biology and Technology, 85: 109-115.
Spadaro, D. and Gullino, M.L. (2004). State of the art and future prospects of the biocontrol of postharvest fruit diseases. International Journal of Food Microbiology, 91: 185-194.
Terry, L.A. and Joyce, D.C. (2004). Elicitors of induced disease resistance in postharvest horticultural crops: a brief review. Postharvest Biology and Technology, 32: 1-13.
Tobudic, S., Kratzer, C. and Presterl E. (2010). Azole-resistant Candida spp.-emerging pathogens? Mycoses, 55: 24-32.
Vico, I., Duduk, N., Vasić, M. and Nikolić, M. (2014). Identification of Penicillium expansum causing postharvest blue mold decay of apple fruit. Pesticides and Phytomedicine, 29: 257-266.
Wang, X., Zhang, X., Sun, M., Wang, L., Zou, Y., Fu, L., Han, C., Li, A., Li, L., Zhu, C. (2022). Impact of vanillin on postharvest disease control of apple. Frontiers in Microbiology, 13:979737.
Zhong, L., Carere, J., Lu, Z., Lu, F. and Zhou, T. (2018). Patulin in apples and apple-based food products: The burdens and the mitigation strategies. Toxins, 10:475.
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Amini, M., Safaie, N., Salmani, M.J. and Shams-Bakhsh, M. (2012). Antifungal activity of three medicinal plant essential oils against some phytopathogenic fungi. Trakia Journal of Sciences, 10: 1-8. [In Persian].
Bradford, M.M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry, 72: 248-254.
Cheng, H., Mou, Z., Wang, W., Zhang, W., Wang, Z. and Zhang, M. (2019). Chitosan-catechin coating as an antifungal and preservable agent for postharvest Satsuma oranges. Journal of Food Biochemistry, 43:e12779.
Cindi, M.D., Sivakumar, D., Romanazzi, G. and Soundy, P. (2016). Differential defense responses and brown rot control after essential oil fumigation in two Prunus persica cultivars during storage. Postharvest Biology and Technology, 19: 9-17.
De Capdeville, G., Beer, S.V., Wilson, C.L., and Aist, J.R. (2002). Alternative disease control agents induce resistance to blue mold in harvested red delicious apple fruit. Phytopathology. 92: 900-908.
Droby, S., Wsiniewski, M., Ei-Ghaouth, A. and Wilson, C. (2003). Biological control of postharvest diseases of fruits and vegetables: current achievements and future challenges. Acta Horticulture, 628: 703-713.
El-Ghaouth, A., Wilson, C.L. and Wisniewski, M. (2003). Control of postharvest decay of apple fruit with Candida saitoana and induction of defense responses. Phytopathology, 93: 344-348.
El-Ghaouth, A., Smilanick, J.L., Wisniewski, M. and Wilson, C.L. (2000). Improved control of apple and citrus fruit decay with a combination of Candida saitoana and 2-deoxy-D-glucose. Plant Disease, 84: 249-253.
Fajardo, J.E., McCollum, T.G., McDonald, R.E. and Mayer, R.T. (1998). Differential induction of proteins in orange Flavedo by biologically based elicitors and challenged by Penicillium digitatum Sacc. Biological Control, 13:143-151.
Gandomi Nasr-Abadi, H., Misaghi, A., Akhoundzadeh Basti, A. and Khosravi, A.R. (2008). Effects of Zataria multiflora Boiss essential oil on Aspergillus flavus. Journal of Medical Plants. 7: 45-451. [In Persian].
Gholamnejad, J. (2017). Effect of plant extracts against apple gray mold caused by Botrytis cinerea. Applied Microbiology in Food Industries, 3: 53-66.
Gholamnejad, J., Etebarian, H.R. and Sahebani N. (2010). Biological control of apple blue mold with Candida membranifaciens and Rhodotorula mucilaginosa. African Journal of Food Science, 4: 1-7.
Haider, S.A., Ahmad, S., Khan, A.S., Anjum, M.A., Nasir, M. and Naz, S. (2020). Effects of salicylic acid on postharvest fruit quality of “Kinnow” mandarin under cold storage. Scientia Horticulturae, 259: 108843.
Hasani, A., Jalili Marandi, R. and Ghosta, Y. (2009). Use of essential oils in control of grey mold (Botrytis cinerea) infection in of pear fruits. Iranian Journal of Horticultural Science 2009; 40: 85-94.
J.H., Ma, L.J., Wang, D.J., Zhang, M.Y. and Zhou, H.L. (2019). Ferulic acid treatment reinforces the resistance of postharvest apple fruit during gray mold infection. Journal of Plant Pathology, 101: 503-511.
Jiang, A.L., Tian, S.P. and Xu, Y. (2002). Effects of controlled atmosphere with high CO2 concentartions on post-harvest physiology and storability of napoleon sweet cherry. Acta Botanica Sinica, 44: 925-930.
Karimi, A. and Meiners, T. (2021). Antifungal activity of Zataria multiflora Boiss. Essential oils and changes in volatile compound composition under abiotic stress conditions, Industrial Crops and Products, 171: 113888.
Khosravi, A.R., Shokri, H., Sharifrohani, M., Ebrahimzadeh Mousavi, H. and Moosavi, Z. (2012). Evaluation of the antifungal activity of Zataria multiflora, Geranium herbarium, and Eucalyptus camaldolensis essential oils on Saprolegnia parasitica-infected rainbow trout (Oncorhynchus mykiss) eggs. Foodborne Pathogen Disease, 9: 674-679.
Li, S., Jiang, H., Wang, Y., Lyu, L., Prusky, D. and Ji, Y. (2020). Effect of benzothiadiazole treatment on improving the mitochondrial energy metabolism involved in induced resistance of apple fruit during postharvest storage. Food Chemistry, 302:125288.
Loncaric, A., Sarkanj, B., Gotal, A.M., Kovač, M., Nevistić, A., Fruk, G., Skendrović Babojelić, M., Babić, J., Miličević, B. and Kovač, T. (2021). Penicillium expansum Impact and patulin accumulation on conventional and traditional apple cultivars. Toxins (Basel), 4; 13(10):703.
Luciano-Rosario, D., Keller, N.P. and Jurick, W.M. (2020). Penicillium expansum: biology, omics, and management tools for a global postharvest pathogen causing blue mold of pome fruit. Molecular Plant Pathology, 21; 1391-1404.
Magri, A., Curci, M., Battaglia, V., Fiorentino, A. and Petriccione, M. (2023). Essential oils in postharvest treatment against microbial spoilage of the Rosaceae family fruits. Applied Chemistry, 3: 196-216.
Malencic, D., Popovic, M. and Miladinovic, J. (2007). Phenolic content and antioxidant properties of soybean (Glycine max (L.) Merr.) Seeds. Molecules, 12: 576-581.
Mohammadi-Pourfard, A., and Kavoosi, G. (2012). Chemical composition, radical scavenging, antibacterial and antifungal activities of Zataria multiflora Bioss essential oil and aqueous extract. Journal of Food Safety, 32: 326-32.
Naseri, M., Arouiee, H., Golmohammadzadeh, S., Jaafari, M.R. and Neamati, H. (2015). Antifungal effects of Zataria multiflora essential oil on the inhibitory growth of some postharvest pathogenic fungi. Notulae Scientia Biologicae, 7: 412-416.
Noori, N., Yahyaraeyat, R., Khosravi, A.R., Atefi, P., Akhondzadeh Basti, A., and Akrami, F. (2012). Effect of Zataria multiflora Bioss. Essential oil on growth and citrinin production by Penicillium citrinum in culture media and mozzarella cheese. Journal of Food Safety, 32: 445-451.
Ntasiou, P., Samaras, A., Karaoglanidis, G. (2021). Apple fruit core rot agents in Greece and control with succinate dehydrogenase inhibitor fungicides. Plant Disease, 105: 3072-3081.
Oroojalian, F., Kasra-Kermanshahi, R., Azizi, M. and Bassami, M.R. (2010). Phytochemical composition of the essential oils from three Apiaceae species and their antibacterial effects on food-borne pathogens. Food Chemistry, 120: 765-770.
Regnier, T., Combrinck, S., Veldman, W. and Duplooy, W. (2014). Application of essential oils as muti-target fungicides for the control of Geotrichum citri- aurantii and other postharvest pathogens of citrus. Industrial Crops and Products, 61: 151-159.
Sanderson, P.G. and Spotts, R.A. (1995). Postharvest decay of winter pear and apple fruit caused by species of Penicillium. Phytopathology, 85: 103-110.
Shokri, H. and Sharifzadeh, A. (2017). Zataria multiflora Boiss. A review study on chemical composition, antifungal and anti-mycotoxin activities, and ultrastructural changes. Journal of Herbmed Pharmacology, 6: 1-9.
Smith, K., SHewfeltoK, R.L., Maclcan, D.D. and Mehra, l.K. (2013). Effect of postharvest biofumigation on fungal decay, sensory quality, and antioxidant levels of blueberry fruit. Postharvest Biology and Technology, 85: 109-115.
Spadaro, D. and Gullino, M.L. (2004). State of the art and future prospects of the biocontrol of postharvest fruit diseases. International Journal of Food Microbiology, 91: 185-194.
Terry, L.A. and Joyce, D.C. (2004). Elicitors of induced disease resistance in postharvest horticultural crops: a brief review. Postharvest Biology and Technology, 32: 1-13.
Tobudic, S., Kratzer, C. and Presterl E. (2010). Azole-resistant Candida spp.-emerging pathogens? Mycoses, 55: 24-32.
Vico, I., Duduk, N., Vasić, M. and Nikolić, M. (2014). Identification of Penicillium expansum causing postharvest blue mold decay of apple fruit. Pesticides and Phytomedicine, 29: 257-266.
Wang, X., Zhang, X., Sun, M., Wang, L., Zou, Y., Fu, L., Han, C., Li, A., Li, L., Zhu, C. (2022). Impact of vanillin on postharvest disease control of apple. Frontiers in Microbiology, 13:979737.
Zhong, L., Carere, J., Lu, Z., Lu, F. and Zhou, T. (2018). Patulin in apples and apple-based food products: The burdens and the mitigation strategies. Toxins, 10:475.
