Inhibitory effect of plant essential oils on controlling Alternaria species

Yıl 2024, Cilt: 8 Sayı: 2, 468 - 478, 27.06.2024

Oktay Erdoğan

https://doi.org/10.31015/jaefs.2024.2.20

Öz

The use of natural products in the control of fungal diseases in plants is considered an alternative to synthetic fungicides due to their less negative effects on the environment. In this study, in vitro inhibitory effect of plant essential oils (PEOs) of black cumin, cumin, chamomile, cedarwood, and ginger were investigated for controlling two species of Alternaria, including Alternari solani and Alternaria alternata on tomato and cabbage under in vitro conditions, respectively. Aiming to evaluate the mycelial growth of the pathogen, mycelial discs were placed in Petri plates with 0, 500, 1000, 1500, 2000, and 2500 μL/L of PEOs. The experiment was carried out in a randomized plot design with three replications. Chemical analysis of PEO components were determined by Gas Chromatography and Mass Spectrometry methods. A total of 69 chemical compounds were determined in five different PEOs. As the main chemical compounds, Cuminaldehyde was detected in cumin PEO, Sesquithujene was found in ginger PEO, and Eucalyptol (1,8-cineole) was determined in black cumin, chamomile, and cedarwood PEOs. All five PEOs were found to inhibit the growth of Alternaria species in a dose-dependent manner, whereas cumin EO was determined more inhibitory effect against A. solani and A. alternata. Cumin PEO showed the highest effect against Alternaria species because it contains a Cuminaldehyde chemical compound. The lowest inhibition percentage was found in chamomile PEO compared to other PEOs. This study suggested that cumin PEO has the potential as an antifungal agent for controlling of Alternaria diseases.

Anahtar Kelimeler

Essential oil, Alternaria solani, Alternaria alternata, Cuminaldehyde, Eucalyptol, Inhibition

Teşekkür

The authors thank to Prof. Dr. Elif Tozlu (Atatürk University, Faculty of Agriculture, Erzurum, Türkiye) and Prof. Dr. Şener Kurt (Hatay Mustafa Kemal University, Faculty of Agriculture, Hatay, Türkiye) for kindly providing local isolates of A. solani (ET 66) and A. alternata.

Kaynakça

• Ahmad, M. S., & Sinha, K. K. (2002). Mycotoxin contamination of mustard seeds during storage. Indian Phytopathology, 55 (3), 299-302.
• Amini, M., Safaie, N., Salmani, M. J., & Shams-Bakhsh, M. (2012). Antifungal activity of three medicinal plant essential oils against some Phytopathogenic fungi. Trakia Journal of Science, 10 (1), 1-8.
• Anderson, S. (1995). To smell a tree. Journal of Forestry, 93 (3), 10.
• Ayodele, A. O., Akinyosoye, A. F., Arotupin, J. D., Owoyemi, O. O., & Oyindamola, B. A. (2018). Phytochemical screening and antifungal activities of Zingiber officinale (Roscoe) on mycotoxigenic fungi associated with the deterioration of Pennisetum glaucum grains. Journal of Advances in Microbiology, 13 (1), 1-11. https://doi.org/10.9734/JAMB/2018/44730
• Bayan, Y., Yılar, M., & Onaran, A. (2017). Heracleum platytaenium Boiss. ve Myrtus communis L. bitki uçucu yağlarının Alternaria solani Ell. and G. Martin ve Monilia laxa Aderh. and Ruhl. (Honey) üzerine antifungal aktivitesinin araştırılması. Academic Journal of Agriculture, 6 (1), 11-16 (in Turkish).
• Camlica, E., & Tozlu, E. (2019). Biological control of Alternaria solani in tomato. Fresenius Environmental Bullettin, 28, 7092-7100.
• Chaerani, R., & Voorrips, R. E. (2006). Tomato early blight (Alternaria solani): the pathogen, genetics, and breeding for resistance, Journal of General Plant Pathology, 72, 335-347. https://doi.org/10.1007/s10327-006-0299-3
• Chauiyakh, O., EL Fahime, E., Aarabi, S., Ninich, O., Ouchari, L., Bentata, F., Chaouch, A., & Ettahir, A. (2023). In vitro biological control of Cedrus atlantica‘s lignivorous fungi by the extracted essential oils from the infected wood. International Wood Products Journal, 1-9. https://doi.org/10.1080/20426445.2023.2265249
• EL-Hefny, M., Abo Elgat, W. A. A., Al-Huqail, A. A., & Ali, H. M. (2019). Essential and recovery oils from Matricaria chamomilla flowers as environmentally friendly fungicides against four fungi ısolated from cultural heritage objects. Processes, 7 (11), 809. https://doi.org/10.3390/pr7110809
• Feng, W., Chen, J., Zheng, X., & Liu, Q. (2011). Thyme oil to control Alternaria alternata in vitro and in vivo as fumigant and contact treatments. Food Control, 22 (1), 78-81. https://doi.org/10.1016/j.foodcont.2010.05.010
• Feng, W., & Zheng, X. (2007). Essential oils to control Alternaria alternata in vitro and in vivo. Food Control, 18, 1126e1130. https://doi.org/10.1016/j.foodcont.2006.05.017
• Foolad, M. R., Ntahimpera, N., Christ, B. J., & Lin, G. Y. (2000) Comparison between field, greenhouse, and detached-leaflet evaluations of tomato germplasm for early blight resistance. Plant Disease, 84, 967-972. https://doi.org/10.1094/PDIS.2000.84.9.967
• Ghasemi, G., Fattahi, M., Alirezalu, A. & Ghosta, Y. (2019). Antioxidant and antifungal activities of a new chemovar of cumin (Cuminum cyminum L.). Food Science and Biotechnology, 28 (3), 669-677. https://doi.org/10.1007/s10068-018-0506-y
• Gou, Y. N., Aung, S. L. L., Htun, A. A., Huang, C. X., & Deng, J. X. (2022). Alternaria species in section Alternaria associated with iris plants in China. Frontiers in Microbiology, 13, 1036950. https://doi.org/10.3389/fmicb.2022.1036950
• Grati Affes, T., Chenenaoui, S., Zemni, H., Hammami, M., Bachkouel, S., Aidi Wannes, W., Nasraoui, B., Saidani Tounsi, M., & Lasram, S. (2023). Biological control of citrus brown spot pathogen, Alternaria alternata by diferent essential oils. International Journal of Environmental Health Research, 33 (8), 823-836. https://doi.org/10. 1080/09603123.2022.2055748
• Guo, W., Fan, K., Nie, D., Meng, J., Huang, Q., Yang, J., Shen, Y., Tangni E. K., Zhao, Z., Wu, Y., & Han, Z. (2019). Development of a QuEChERS-based UHPLC-MS/MS method for simultaneous determination of six Alternaria toxins in grapes. Toxins, 11 (2), 87. https://doi.org/10.3390/toxins11020087
• Hadizadeh, I., Peivastegan, B., & Kolahi, M. (2009). Antifungal activity of nettle (Urtica dioica L.), colocynth (Citrullus colocynthis L. Schrad), oleander (Nerium oleander L.) and konar (Ziziphus spina-christi L.) extracts on plants pathogenic fungi. Pakistan Journal of Biological Sciences, 12 (1), 58-63. http://dx.doi.org/10.3923/pjbs.2009.58.63.
• Horsfield, A., Wicks, T., Davies, K., Wilson, D., & Paton, S. (2010). Effect of fungicide use strategies on the control of early blight (Alternaria solani) and potato yield. Australasian Plant Pathology, 39, 368-375. https://doi.org/10.1071/AP09090
• Kačániová, M., Galovičová, L., Valková, V., Ďuranová, H., Štefániková, J., Čmiková, N., Vukic, M., Vukovic, N. L., & Kowalczewski, P. Ł. (2022). Chemical composition, antioxidant, ın vitro and ın situ antimicrobial, antibiofilm, and anti-ınsect activity of Cedar atlantica essential oil. Plants, 11 (3), 358. https://doi.org/10.3390/plants11030358
• Karuna, K., Jagadish, K. S., Geetha, K. N., & Shadakshari, Y. G. (2012). Evaluation of efficacy of chemical fungicides and a plant product for the management of Alternaria blight of sunflower. Indian Phytopathology, 65 (3), 305-306. https://www.cabdirect.org/ca bdirect/abstract/20123401603
• Kedia, A., Prakash, B., Mishra, P. K., Dubey, N. K. (2014). Antifungal and antiaflatoxigenic properties of Cuminum cyminum (L.) seed essential oil and its efficacy as a preservative in stored commodities. International Journal of Food Microbiology, 168, 1-7. http://dx.doi.org/10.1016/j.ijfoodmicro.2013.10.008
• Khan, M. M., Khan, R. U., & Mohiddin, F. A. (2007). Studies on the cost-effective management of Alternaria blight of rapeseed-mustard (Brassica spp.). Phytopathology Mediterranean, 46, 201-206. https://doi.org/10.14601/Phytopathol_Mediterr-2158.
• Kirk, W. W. , Abu-El Samen, F. M., Muhinyuza, J. B., Hammerschmidt, R., Douches, D. S., Thill, C. A., Groza, H., & Thompson, A. L. (2005). Evaluation of potato late blight management utilizing host plant resistance and reduced rates and frequencies of fungicide applications. Crop Protection, 24 (11), 961-970. https://doi.10.1016/j.cropro.2004.12.016
• Kumar, A., Suravajhala, R., & Bhagat, M. (2020). Bioactive potential of Cedrus deodara (Roxb.) Loud essential oil (bark) against Curvularia lunata and molecular docking studies. SN Applied Sciences, 2, 1045. | https://doi.org/10.1007/s42452-020-2837-6
• Kumar, M. P., Gowda, D. S., Moudgal, R., Kumar, N. K., Gowda, K. P., & Vishwanath, K. (2013) Impact of fungicides on rice production in India. Fungicides-showcases of integrated plant disease management from around the world. IntechOpen, London.
• Leyva Salas, M., Mounier, J., Valence, F., Coton, M., Thierry, A., & Coton, E. (2017). Antifungal microbial agents for food biopreservation-A review. Microorganisms, 5 (3), 37. https://doi.org/10.3390/microorganisms5030037
• Mafakheri, H., Mirghazanfari, S. M. (2018). Antifungal activity of the essential oils of some medicinal plants against human and plant fungal pathogens. Cellular and Molecular Biology, 64 (15), 13-19. http://dx.doi.org/10.14715/cmb/2017.64.15.3
• Marak, T. R., Ambesh, B. S., & Srikanta, D. (2014). Cultural, morphological and biochemical variations of Alternaria solani causing diseases on solanaceous crops. The Bioscan, 9 (3), 1295-1300.
• Meena, M., Gupta, S. K., Swapnil, P., Zehra, A., Dubey, M. K., & Upadhyay, R. S. (2017) Alternaria toxins: potential virulence factors and genes related to pathogenesis. Frontiers in Microbiology, 8, 1451. https://doi.org/ 10.3389/fmicb.2017.01451
• Morcia, C., Malnati, M., & Terzi, V. (2012). In vitro antifungal activity of terpinen-4-ol, eugenol, carvone, 1,8-cineole (eucalyptol) and thymol against mycotoxigenic plant pathogens. Food additives & Contaminants. Part A, Chemistry, Analysis, Control, Exposure & Risk Assessment, 29 (3), 415-422. https://doi.org/10.1080/19440049.2011.643458
• Moumni, M., Romanazzi, G., Najar, B., Pistelli, L., Ben Amara, H., Mezrioui, K., Karous, O., Chaieb, I., & Allagui, M. B. (2021). Antifungal activity and chemical composition of seven essential oils to control the main seedborne fungi of cucurbits. Antibiotics, 10, 104. https://doi.org/10.3390/ antibiotics10020104
• Mukai, A., Takahashi, K., & Kofujita, H. (2019). Antitermite and antifungal activities of thujopsene natural autoxidation products. European Journal of Wood and Wood Products, 77, 311-317. https://doi.org/10.1007/s00107-018-1370-4
• Namanda, S., Olanya, O. M., Adipala, E., Hakiza, J. J., ElBedewy, R., Bagshari, A. S., & Ewell, P. (2004). Fungicide application and host resistance for potato late blight management: benefits assessment from on-farm studies in S.W. Uganda. Crop Protection, 23, 1075-1083. https://doi.org/10.1016/j.cropro.2004.03.011
• Naz, H. (2011). Nigella sativa: the miraculous herb. Pakistan Journal of Biochemistry and Molecular Biology, 44 (1), 44-48.
• Nerio, L. S., Olivero-Verbel, J., & Stashenko, E. (2010). Repellent activity of essential oils: a review. Bioresource Technology, 101, 372-378. http://dx.doi.org/10.1016/j.biortech. 2009.07.048.
• Pandey, S., Giri, V. P., Tripathi, A., Kumari, M., Narayan, S., Bhattacharya, A., Srivastava, S., & Mishra, A. (2020). Early blight disease management by herbal nanoemulsion in Solanum lycopersicum with bio-protective manner. Industrial Crops and Products, 150, 112421. https://doi.org/10.1016/j.indcrop.2020.112421
• Patni, C. S., Kolte, S. J., & Awasthi, R. P. (2005). Efficacy of botanicals against Alternaria blight (Alternaria brassicae) of mustard. Indian Phytopathology, 58 (4), 426-430.
• Paulitz, T. C., & Belanger, R. R. (2001). Biological control in greenhouse systems. Annual Review of Phytopathology, 39, 10333. https://doi.org/10.1146/annurev.phyto.39.1.103
• Porcino, M. M., Oliveira, V., da Silva, H. F., de Souza, M., & Do Nascimento, L. C. (2023). Essential oils in the management of Alternaria alternata f. sp. citri in ‘Dancy’tangerine fruits. Revista Caatinga, 36, 291-299. https://doi.org/10.1590/1983-21252023v36n206rc
• Rahmah, A. N., Mostafa, A. A., Abdel-Megeed, A., Yakout, S. M., & Hussein, S. A. (2013). Fungicidal activities of certain methanolic plant extracts against tomato phytopathogenic fungi. African Journal of Microbiology Research, 7 (6), 517-524. https://doi.org/10.5897/AJMR12.1902
• Regnault-Roger, C., Vincent, C., & Arnason, J. T. (2012). Essential oils in insect control: low-risk products in a high-stakes world. Annual Review of Entomology, 57, 405-424. https://doi.org/10.1146/annurev-ento-120710-100554
• Rizwana, H. (2015). Exploiting antifungal potential of ginger for the management of Alternaria alternata, the cause of leaf spot disease of spinach. Mycopath, 13 (2), 97-104.
• Romagnoli, C., Andreotti, E., Maietti, S., Mahendra, R., & Mares, D. (2010). Antifungal activity of essential oil from fruits of Indian Cuminum cyminum. Pharmaceutical Biology, 48 (7), 834-838. https://doi.org/10.3109/13880200903283715
• Sağlan, Z., Ceylan, Y., Çelik Turgut, G., & Erdogan, O. (2022). Antifungal effect of some plant essential oils against verticillium wilt (Verticillium dahliae Kleb.) in cotton. Journal of Scientific and Engineering Research, 9 (7), 55-65.
• Saharan, G. S., Mehta, N., Meena, P. D., & Dayal, P. (2016). Alternaria diseases of crucifers: biology, ecology and disease management. Gateway East, Springer. Singapore.
• Sazvar, E., Jahani, M., Aminifard, M. H., & Hosseini, S. A. (2022) In vitro and in vivo control of Alternaria alternata in barberry (Berberis vulgaris) by some essential oils. Erwerbs-Obstbau, 64 (3), 413-423. https://doi.org/10.1007/s10341-022-00645-2
• Semiz, G., Çelik, G., Gönen, E., & Semiz, A. (2016). Essential oil composition, antioxidant activity and phenolic content of endemic Teucrium alyssifolium Staph. (Lamiaceae). Natural Product Research, 30 (19), 2225-2229. https://doi.org/10.1080/14786419.2016.1149703
• Seyedjavadi, S. S., Khani, S., Eslamifar, A., Ajdary, S., Goudarzi, M., Halabian, R., Akbari, R., Zare-Zardini, H., Imani Fooladi, A. A., Amani, J., & Razzaghi-Abyaneh, M. (2020). The Antifungal peptide MCh-AMP1 derived from Matricaria chamomilla inhibits Candida albicans growth via inducing ROS generation and altering fungal cell membrane permeability. Frontiers in Microbiology, 10, 3150. https://doi.org/10.3389/fmicb.2019.03150
• Sharma, R. L., Ahir, R. R., Yadav, S. L., Sharma, P., & Ghasolia, R. P. (2021). Effect of nutrients and plant extracts on Alternaria blight of tomato caused by Alternaria alternata. Journal of Plant Diseases and Protection, 128, 951-960. https://doi.org/10.1007/s41348-021-00485-4
• Sheetal, V., & Singh, S P. (2008). Current and future status of herbal medicines. Veterinary World, 1 (11), 347-350.
• Sitara, U., Niaz, I., Naseem, J., & Sultana, N. (2008). Antifungal effect of essential oils on in vitro growth of pathogenic fungi. Pakistan Journal of Botany, 40, 409-414.
• Smith, C. T. (2001). What are fungi? In The Mycota. Edited by: McLaughlin DJ, McLaughlin EG, Lemke PA. New York: Springer.
• Sokovi’c, M., & van Griensven, J. L. D. (2006). Antimicrobial activity of essential oils andtheir components against the three major pathogens of the cultivated button mushroom, Agaricus bisporus. European Journal of. Plant Pathology, 116 (3), 211-224. https://doi.org/10.1007/s10658-006-9053-0
• Soliman, K. M., & Badeaa, R. I. (2002). Effect of oil extracted from some medicinal plants on different mycotoxigenic fungi. Food and Chemical Toxicology, 40, 1669-1675. https://doi.org/10.1016/S0278-6915(02)00120-5
• Soylu, S., Kara, M., Uysal, A., Gümüş, Y., Soylu, E. M., Kurt, Ş., Üremiş, İ., & Sertkaya, E. (2024). Determination of fungal and bacterial disease agents on significant brassicaceous vegetable species grown in Hatay province. KSU Journal of Agricultural and Natural, 27(4), 839-855. https://doi.org/10.18016/ksutarimdoga.vi.1383042
• Soylu, S., Kara, M., Soylu, E. M., Uysal, A., & Kurt, Ş. (2022). Geotrichum citri-aurantii’nin sebep olduğu turunçgil ekşi çürüklük hastalığının biyolojik mücadelesinde endofit bakterilerin biyokontrol potansiyellerinin belirlenmesi. Journal of Tekirdag Agricultural Faculty, 19 (1), 177-191 (in Turkish). https://doi.org/10.33462/jotaf.944704
• Swart, S. H., Wingfield, M. J., Swart, W. J., & Schutte, G. C. (1998). Chemical control of Alternaria brown spot on minneola tangelo in South Africa. Annals of Applied Biology, 133, 17-30. https://doi.org/10.1111/j.1744-7348.1998.tb05798.x
• Tian, J., Ban, X., Zeng, H., He, J., Chen, Y., & Wang, Y. (2012). The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. PLoS ONE, 7 (1), e30147. https://doi.org/10.1371/journal.pone.0030147
• Tsuge, T., Harimoto, Y., Akimitsu, K., Ohtani, K., Kodama, M., Akagi, Y., Egusa, M., Yamamoto, M., & Otani, H. (2013) Hostselective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiology Reviews, 37 (1), 44-66. https://doi.org/10.1111/j.1574-6976.2012.00350.x
• Yeşil Çeliktaş, O., Hames, Kocabaş, E. E., Bedir, E., Vardar Sukan, F., Özek, T., & Baser, K. H. C. (2007). Antimicrobial activities of methanol extracts and essential oils of Rosmarinus officinalis, depending on location and seasonal variations. Food Chemistry, 100 (2), 553-559. https://doi.org/10.1016/j.foodchem.2005.10.011