Evaluation of antifungal activity of some natural essential oils against fungal pathogens associated with maize grains
Article Sidebar
Main Article Content
Abstract
Mycotoxin-producing moulds which considered as common maize grains contaminants are presented in the genera Fusarium, Aspergillus and Penicillium. One of the natural and safe ways to protect grains from mould contamination is the use of essential oils. The antifungal activity of thyme, citral, methyl anthranilate, rosemary and clove, essential oils (EOs) against Fusarium. moniliforme, Aspergillus niger, Penicillium sp., Aspergillus flavus and Aspergillus terreus was evaluated in direct contact assay. All EOs showed significant impact on mycelial growth and spore germination inhibition. Thyme showed the best inhibitory effect while, methyl anthranilate and rosemary were the most effective EOs for spore germination inhibition. The effect of EOs added to grains in different application methods (volatile and carrier contact assays) were evaluated. In volatile assay, frequency of F. moniliforme and A. niger isolated from maize grains was greatly inhibited by rosemary, P. sp. was most affected by methyl anthranilate, and A. flavus growth reduced by thyme. On the other hand, frequency of F. moniliforme and Penicillium. sp. were greatly inhibited by the clove at EC50 =4.5009 and EC90 =6.9351mg/mL, while A. niger was most affected by citral as well as rosemary and methyl anthranilate leaded to the major frequency reduction of A. flavus. Our results cleared that vapor contact assay had stronger antifungal activity as a post-harvest treatment than carrier contact assay. These results suggested that fungi can be controlled by EOs, especially clove and thyme oils.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Al-Dhabi, N. A., Ghilan, A. K. M., Arasu, M. V. and Duraipandiyan, V. (2018). Green biosynthesis of silver nanoparticles produced from marine Streptomyces sp. Al-Dhabi-89 and their potential applications against wound infection and drug resistant clinical pathogens. Journal of Photochemistry and Photobiology B: Biology, 189:176-184.
Al-Dhabi, N. A., Ghilan, A. K. M., Esmail, G. A., Arasu, M. V., Duraipandiyan, V. and Ponmurugan, K. (2019). Bioactivity assessment of the Saudi Arabian Marine Streptomyces sp. Al-Dhabi -90, metabolic profiling and its in vitro inhibitory property against multidrug resistant and extended-spectrum beta-lactamase clinical bacterial pathogens. Journal of Infection and Public Health, 12:549-556.
Amiri, A., Dugas, R., Pichot, A. L. and Bompeix, G. (2008). In vitro and in vitro activity of eugenol oil (Eugenia caryophylata) against four important postharvest applied pathogens. International Journal of Food Microbiology, 126:13-19.
Anonymous (2018). The Central Administration of Agricultural Economics. In: Year book of statistics and economics, The Ministry of Agriculture and Land Reclamation pp. 168.
Anthony S., Abeywickrama K. and Wijeratnam, S. W. (2003). The effect of spraying essential oils of Cymbopogon nardus, Cymbopogon flexuosus and Ocimum basilicum on postharvest diseases and storage life of Embul banana. journal of horticultural science & biotechnology, 78:780-785.
Arrebola, F., Pérez-Marín, C. C. and Santiago-Moreno, J. (2010). Limitation of seasonality in reproductive parameters of Mediterranean bucks using photoperiod treatment. Small Ruminant Research, 89:31-35.
Baratta, T. M., Dorman, D. J. H., Deans, G. S., Figueiredo, C. A., Barroso, G. J. and Ruberto, G. (1998). Antimicrobial and antioxidant properties of some commercial essential oils. Flavour and Fragranace Journal, 13:235-244.
Barnett, H. L. and Hunter, B. B. (1986). Illustrated genera of fungi. In: imperfecti 3rdedition, Burgess Publishing Company, Minnesota, U.S.A. 241 p.
Bill, M., Sivakumar, D., van Rooyan, Z. and Mavuso, Z. S. (2015). New methods of postharvest disease control: Using Thyme oil fumigation. South African Avocado Growers’ Association Year Book, 38:98-104.
Bluma, R. and Etcheverry, M. (2008). Application of essential oils in maize grain: impact on Aspergillus section Flavi growth parameters and aflatoxin accumulation. Food Microbiology, 25:324-334.
Bluma, R., Landa, M. F., Etcheverry, M. (2009). Impact of volatile compounds generated by essential oils on Aspergillus section Flavi growth parameters and aflatoxin accumulation. Journal of the Science of Food and Agriculture, 89:1473-1480.
Boukaew, S., Prasertsan, P., Sattayasamitsathit, S. (2017). Evaluation of antifungal activity of essential oils against aflatoxigenic Aspergillus favus and their allelopathic activity from fumigation to protect maize seeds during storage. Industrial Crops and Products, 97:558-566.
Bozik, M., Císarová, M., Tancinová, D., Kourimská, L., Hleba, L. and Kloucek, P. (2017). Selected essential oil vapours inhibit growth of Aspergillus spp. in oats with improved consumer acceptability. Industrial Crops and Products, 98:146-152.
Burt, S. (2004). Essential oils: their antimicrobial properties and potential applications in foods-a review. International Journal of Food Microbiology, 94:223-253.
Cakir, A., Kordali, S., Zengin, H., Izumi, S. and Hirata, T. (2004). Composition and antifungal activity of essential oils isolated from Hypericum hyssopifolium and Hypericum heterophyllum. Flavour and Fragrance Journal, 19:62-68.
Calo, J. R., Crandall, P. G., O’Bryan, C. A. and Ricke, S. C. (2015). Essential oils as antimicrobials in food systems-a review. Food Control, 54:111-119.
Carson, C. F., Mee, B. J. and Riley, T. V. (2002). Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphyclococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assay and electron microscopy. Antimicrobial Agents Chemotherapy, 46:1914-1920.
Castlellarie, C., Marcos, F. V., Mutti, J., Cardoso, L. and Bartosik, R. (2010). Toxigenic fungi in Corn (maize) stored in hermetic plastic bags. National institute of agricultural Technologies Mardel Plata University Argentina, pp.115-297.
Chang, Y., Harmon, P. F., Treadwell, D. D., Carrillo, D., Sarkhosh, A. and Brecht, J. K. (2022). Biocontrol Potential of Essential Oils in Organic Horticulture Systems: From Farm to Fork. Frontiers Nutrition, 8:805138.
Čvek, D., Markov, K., Frece, J., Dragiˇcevi´c, T., Majica, M., and Delas, F. (2010). Growth inhibition of Aspergillus ochraceus ZMPBF 318 and Penicillium expansum ZMPBF 565 by four essential oils. Archives of Industrial Hygiene and Toxicology, 61:191-196.
Daniel, C. K., Lennox, C. L. and Vries, F. A. (2015). In-vitro effects of garlic extracts on pathogenic fungi Botrytis cinerea, Penicillium expansum and Neofabraea alba. South African Journal of Science, 111:1-8.
Dhingra, O. D. and Sinclair, J. B. (1985). Basic plant pathology methods. CRC Press.
Elgorban, A. M., Bahkali, A. H., El Metwally, M. A., Elsheshtawi, M., Abdel Wahab, M. A. (2015). In vitro antifungal activity of some plant essential oils. International Journal of Pharmacology, 11:56-61.
Farag, R. S., Daw, Z. Y., Hewedi, F. M. B. and El-Baroty, G. S. A. (1989). Antimicrobial activity of some Egyptian spice essential oils. Journal of Food Protection, 52:665-667.
Gilman, J. C. (1957). A manual of soil fungi. 2nd ed. Ames, Iowa: The Iowa State University Press, pp.450.
Golob, P., Kutukwa , N., Devereau, A., Bartosik, R. E. and Rodriguez, J. C. (2004). Maize. In: Hodges R, Farrell G, editors. Crop post-harvest. Science and Technology: Ames, Iowa. Blackwell Publishing Ltd, 2:(2).
Gong, Y., Huang, Y., Zhou, L., Shi, X., Guo, Z., Wang, M.and Jiang, W. (2009). Chemical composition and antifungal activity of the fruit oil of Zanthoxylum bungeanum Maxim. (Rutaceae) from China. Journal of Essential Oil Research, 21:174-178.
Gormez, A., Bozari, S., Yanmis, D., Gulluce, M., Agar, G., Sahin, F. (2016). The use of essential oils of Origanum rotundifolium as antimicrobial agent against plant pathogenic bacteria. Journal of Essential Oil Research, 19:656-663.
Jacob, S. R., Arunkumar, M. B., Gopal, M., Srivastava, C. and Sinha, S. N. (2009). An analysis of the persistence and potency of film-coated seed protectant as influenced by various stor¬age parameters. Pest Management Science, 65:817-822.
Karaca, G., Bilginturan, M. and Olgunsoy, P. (2017). Effects of Some Plant Essential Oils against Fungi on Wheat Seeds. Indian Journal of Pharmaceutical Education and Research, 51:385-388.
Kavitha, K. S. and Satish, S. (2016). Bio Prospecting of some medicinal plants explored for antifungal activity. Pharmacognosy Journal, 8:59-65.
Keawkham, T., Siri, B. and Hynes, R. K. (2014). Effect of polymer seed coating and seed dressing with pesticides on seed quality and storability of hybrid cucumber. Australian Journal of Crop Science, 8:1415-1420.
Khan, A. M. S. and Ahmad, I. (2011). In vitro antifungal, anti-elastase and anti-keratinase activity of essential oils of Cinnamomum, Syzygium and Cymbopogon species against Aspergillus fumigatus and Trichophyton rubrum. Phytomedicine, 19:48-55.
Kumar, P., Mishra, S., Kumar, A., Sharma, A. K. (2016). Antifungal efficacy of plant essential oils against stored grain fungi of Fusarium spp. Journal of Food Science Technology, 53:3725-3734.
Kumar, V., Mathela, C. S., Tewari, A. K., Bisht, K. S. (2014) In vitro inhibition activity of essential oils from some Lamiaceae species against phytopathogenic fungi. Pesticide Biochemistry and Physiology, 114:67-71.
Kyenpia, E. O., Namo, O. A. T., Gikyu, S.W. and Ifenkwe, O. P. (2009). A comparative study of the biochemical composition of some varieties of maize (Zea mays) grown in Nigeria. Nigeria Journal of Botany, 22:291-296.
Leslie, J. F. and Summerell, B. A. (2006). The Fusarium laboratory manual. UK: Blackwell Publishing Ltd. 388 p.
Liu, H., Wang, J., Zhao, J., Lu, S., Wang, J., Jiang, W., Ma, Z. and Zhou, L. (2009). Isoquinoline alkaloids from Macleaya cordata active against plant microbial pathogens. Natural Product Communications, 4:1557-1560.
Lopez-Reyes, J. G., Spadaro, D., Prelle, A., Garibaldi, A., Gullino, M. L., (2013). Efficacy of plant essential oils on postharvest control of rots caused by fungi on different stone fruits in vivo. Journal of Food Protection, 76:631-639.
Martínez, J. A. (2012). Natural fungicides obtained from plants. Chapter 1. In: Dhanasekaran, D., Thajuddin, N., Panneerselvam , A. (Eds). Fungicides for plant and animal diseases. Europe: InTech, pp.3-28.
Moodley, S. (2015). The application of plant based pesticides in sustainable agriculture. Research & Technology bulletin.
Naeini, A., Ziglari, T., Shokri, H. and Khosravi, A. R. (2010). Assessment of growth inhibiting effect of some plant essential oils on different Fusarium isolates. Journal of Medical Mycology, 20:174-178.
Nelson, P. E., Toussoun, T. A. and Marasas, W. F. O. (1983). Fusarium species. An illustrated manual for identification. University Park: Pennsylvania State University Press, pp.193.
Nesci, A., Montemarani, A., Passone, M. A. and Etcheverry, M. (2011). Insecticidal activity of synthetic antioxidant, natural phytochemicals, and essential oils against an Aspergillus section Flavi vector (Oryzaephilus surinamensis L.) in microcosm. Journal of Pest Science, 84:107-115.
Nguefack, J., Leth, V., Lekagne Dongmo, J. B., Torp, J., Amvam Zollo, P. H. and Nyasse, S. (2008). Use of Three Essential Oils as Seed Treatments Against Seed-borne Fungi of Rice (Oryza sativa L.). American-Eurasian Journal of Agricultural and Environmental Sciences, 4:554-560.
Nguefack, J., Nguikwie, S. K., Fotio, D., Dongmo, B., Leth, V., Nkengfack, A. E. and Zollo, A. B. H. (2007). Fungicidal potential of essential oils and fractions 31. from Cymbopogon citratus, Ocimum gratissimum and Thymus vulgaris to control Alternaria padwickii and Bipolaris oryzae, two seed-borne fungi of rice. Journal of Essential oil Research, 19:581-587.
Olga, P. and Tibor, P. (2015). Maize-Pathogen Interactions: An Ongoing Combat from a Proteomics Perspective. International journal of molecular sciences, 16:28429-28448.
Ortiz, R., Taba, S., Chavez Tovar, V. H., Mezzalama, M., Xu, Y., Yan, J. and Crouch J. H. (2010). Conserving and Enhancing Maize Genetic Resources as Global Public Goods– A Perspective from CIMMYT. Crop Science, 50:13-28.
Ozcan, M. and Boyraz, N. (2000). Antifungal properties of some herb decoctions. European Food Research and Technology, 212:86-88.
Passone, M. A., Girardi, N. S., and Etcheverry, M. (2012). Evaluation of the control ability of five essential oils against Aspergillus section Nigri growth and ochratoxin A accumulation in peanut meal extract agar conditioned at different water activities levels. International Journal of Food Microbiology, 159:198-206.
Paster, N., Menasherov, M., Ravid, U. and Juven, B. (1995). Antifungal activity of oregano and thyme essential oils applied as fumigants against fungi attacking stored grains. Journal of Food Protection, 58:81-85.
Pawar, V. C. and Thaker, V. S. (2006): In vitro efficacy of 75 essential oils against Aspergillus niger. Mycoses, 49:316-323.
Perczak, A., Gwiazdowska, D., Marchwińska, K., Juś, K., Gwiazdowski, R. and Waśkiewicz, A. (2019). Antifungal activity of selected essential oils against Fusarium culmorum and F. graminearum and their secondary metabolites in wheat seeds. Archives of Microbiology, 201:1085-1097.
Perczak, A., Juś, K., Marchwińska, K., Gwiazdowska, D., Waśkiewicz, A. and Goliński, P. (2016). Degradation of zearalenone by essential oils under in vitro conditions. Frontiers in Microbiology, 7:1224.
Prakash, B., Kedia, A., Mishra, P. K. and Dubey, N. K. (2015). Plant essential oils as food preservatives to control moulds, mycotoxin contamination and oxidative deterioration of agri food commodities potentials and challenges. Food Control, 47:381-391.
Pushpavathi, D., Shilpa, M., Petkar, T., Siddiqha, A., and Kekuda, P. T. (2017). Evaluation of antifungal activity of some plants against seed-borne fungi. Scholars Journal of Agriculture and Veterinary Sciences, 4: 155-159.
Quiroga, E. N., Sampietro, A. R. and Vattuone, M. A (2001). Screening antifungal activities of selected medicinal plants. Journal of Ethnopharmacology, 74:89-96.
Ramadan, K. M., Ali, M. K., El-Gobashy, R. E., Georghiou, P. E., Ali, N. A. and Zaher, E. A. (2007). Application of Volatile Fractions from Ageratum houstonianum and Tagetes erecta as safe Management of some Root Phytopatogenic Fungi. Arab Universities Journal of Agricultural Sciences, 15:185-193.
Russo, M., Galleti, G. C., Bocchini, P. and Carnacini, A. (1998). Essential oils chemical composition of wild population of Italian oregano spice (Origanum vulgare spp. hirtum (Link) letswaard): a preliminary evaluation of their use in chemotaxonomy by cluster analysis: 1. Influrescences. Journal of Agricultural and Food Chemistry, 46:3741-3746.
Sahab, A. F., Aly, S., Hathout, A.S., Ziedan, E. S. H. and Sabry, B. A. (2014). Application of some plant essential oils to control Fusarium isolates associated with freshly harvested maize in Egypt. Journal of Essential Oil-Bearing Plants, 17:1146-1155.
Santamarina, M. P., Rosello, J., Gimenez, S. and Blazquez, M. A. (2016). Commercial Laurus nobilis L. and Syzygium aromaticum L. Merr. & Perry essential oils against post harvest phytopathogenic fungi on rice. LWT - Food Science and Technology, 65:325-332.
Santos, F., Medina, P. F., Lourenção, A. L., Parisi, J. D. and Godoy, I. J. (2016). Damage caused by fungi and insects to stored peanut seeds before processing. Bragantia, 75:184-192.
Sawinska, Z., Świtek, S., Głowicka-Wołoszyn, R. and Kowalczewski, P. Ł. (2020). Agricultural practice in Poland before and after mandatory IPM Implementation by the European Union. Sustainability, 12:1107.
Shahbandeh, M. (2020). Corn - Statistics & Facts. Statista. Available from: https://www.statista.com/topics/986/ corn/#dossierSummary__chapter4/.
Shannon, E. M., Milillo, S. R., Johnson, M. G. and Ricke, S. C. (2011). Efficacy of cold pressed terpeneless valencia oil and its primary components on inhibition of Listeria species by direct contact and exposure to vapors. Journal of Food Science, 76:500-503.
Sinha, K. K., Sinha, A. K. and Prasad, G. (1993). The effect of clove and cinnamon oils on growth of and aflatoxin production by Aspergillus flavus. Lett. Journal of Applied Microbiology, 16:114-117.
Skandamis, P. N. and Nychas, G. J. E. (2000). Development and evaluation of a model predicting to the survival of Escherichia coli O157H7 NCTC 12900 in homemade eggplant salad at various temperatures, pHs and oregano essential oils concentration. Applied and Environmental Microbiology, 66:1646-1653.
Soliman, K. M. and Badeaa, R. I. (2002). Effect of oil extracted from some medicinal plants on different mycotoxigenic fungi. Food and Chemical Toxicology, 40:1669-1675.
Solorzano Santos, F. and Miranda Novales, M. G. (2012). Essential oils from aromatic herbs as antimicrobial agents. Current Opinion in Biotechnology 23:136-141.
Somda, I., Leth, V. and Sereme, P., (2007). Antifungal effect of Cymbopogon citratus, Eucalyptus camaldulensis and Azadirachta indica oil extracts on sorghum seed borne fungi. Asian Journal of Plant Sciences, 6:1182-1189.
Song, W., Zhou, L., Yang, C., Cao, X., Zhang, L. and Liu, X (2004). Tomato Fusarium wilt and its chemical control strategies in a hydroponic system. Crop Protection, 23:243-247.
Spadaro, D., Herforth-Rahmé, J. and van der, Wolf J. (2017). Organic seed treatments of vegetables to prevent seedborne diseases. Proc. III International Symposium on Organic Greenhouse Horticulture. Acta Horticulturae, 1164:23-32.
Suzuki, E. Y., Soldati, P. P., Chaves, M. G. A. M. and Raposo N. R. B. (2015). Essential Oil from Origanum vulgare Linnaeus: An Alternative against Microorganisms responsible for Bad Perspiration Odour. Journal of Young Pharmacists, 7:12-20.
Tassou, C., Koutsoumanis, K. and Nychas, G. J. E. (2000). Inhibition of Salmonella enteritidis and Staphylococcus aureus in nutrient broth by mint essential oil. Food Research International, 33:273-280.
Thanaboripat, D., Mongkontanawur, N., Suvathi, Y. and Ruangrattanamatee, V., (2004). Inhibition of aflatoxin production and growth of Aspergillus flavus by citronella oil. KMITL Science And Technology Journal, 4:1.
Thom, C. and Raper, K. B. (1945). A Manual of the Aspergilli. Williams & Wilkins. Baltimore, USA 373 p.
Tripati, P. and Dubey, N. K., (2004). Exploitation of natural products as an alternative strategy to control postharvest fungal rotting of fruit and vegetables. Postharvest Biology and Technology, 32:235-245.
Tzortzakis, N. G. and Economakis, C. D. (2007). Antifungal activity of lemongrass (Cympopogon citratus L.) essential oil against key postharvest pathogens. I Innovative Food Science and Emerging Technologies, 8:253-258.
Ultee, A., Bennink, M. H. J. and Moezelaar, R., (2002). The phenolic hydroxyl group of carvacrol is essential for action against the foodborne pathogens Bacillus cereus. Applied and Environmental Microbiology, 68:1561-1568.
Velluti, A., Sanchis, V., Ramos, A. J., Egido, J., and Marín, S. (2003). Inhibitory effect of cinnamon, clove, lemongrass, oregano and palmarosa essential oils on growth and fumonisin B1 production by Fusarium proliferatum in maize grain. International Journal of Food Microbiology, 89:145-154.
Vergis, J., Gokulakrishnan, P., Agarwal, R. K., and Kumar, A. (2015). Essential oils as natural food antimicrobial agents: a review. Critical Reviews in Food Technology, 55:1320-1323.
Vess, K. A., Smith, G. W. and Haschelh, W. M. (2007). Fumonisins: Toxicokinetics mechanism of action and toxicity. Animal feed science and Technology, 137:299-325.
Vignesh, S., Dahms, H. U., Muthukumar, K., Vignesh, G. and James, R. A. (2016). Biomonitoring along the Tropical Southern Indian Coast with Multiple Biomarkers. PLoS ONE, 11(12).
Viollon, C. and Chaumont, J. P., (1994). Antifungal properties of essential oils and their main components upon Cryptococcus neoformans. Mycopathologia, 128:151-153.
Waithaka, P. N., Gathuru, E. M., Githaiga, B. M., Muthoni, J. W. and Laban, L. T. (2007). Control of Maize Fungal Diseases using Essential Oils Extracted from Rosemary and Eucalyptus in Egerton University Main Campus Njoro, Kenya. International Journal of Research and Technology, 6:5-11.
Wang, L., Liu, B., Jin, J., Ma, L., Dai, Z., Pan, L., Liu, Y., Zhao, Y. and Xing, F. (2019). The Complex Essential Oils Highly Control the Toxigenic Fungal Microbiome and Major Mycotoxins During Storage of Maize. Frontiers in Microbiology, 10:1643.
Wang, J., Zhao, J., Liu, H., Zhou, L., Liu, Z., Wang, J., Han, J., Yu, Z. and Yang, F. (2010). Chemical analysis and biological activity of the essential oils of two valerianaceous species from China: Nardostachys chinensis and Valeriana officinalis. Molecules, 15:6411-6422.
Yilmaz, M., Baysal, Ö. and Sīlme, R. S. (2021). The effect of a seed coating with Origanum vulgare essential oil on Clavibacter michiganensis subsp. Michiganensis. Plant Protection Science, 57:217-225.
Yuan, Y., Xing, F., and Liu, Y. (2013). Role of essential oils in the inhibition of fungal growth and mycotoxin accumulation. Journal of Nuclear Agricultural. Science, 27:1168-1172.
Zeng, D., Mei, X. and Wu, J. (2010). Effects of an environmentally friendly seed coating agent on combating head smut of corn caused by Sphacelotheca reiliana and corn growth. Journal of Agricultural Biotechnology and Sustainable Development, 2:108-112.
