A comparative assessment of antifungal activity of essential oils of five medicinal plants from Tunisia

Taycir Grati Affes; Salma Lasram; Majdi Hammami; Walid Yeddes; Wissem Aidi Wannes; Saber Khammassi; Bouzid Nasraoui; Moufida Saidani Tounsi; Nehla Labidi Ben Hmida

doi:10.29228/ijpbp.4

Authors

Taycir Grati Affes Borj-Cedria Biotechnology Center, Laboratory of Aromatic and Medicinal Plants, BP901, Hammam-Lif 2050, Tunisia https://orcid.org/0000-0003-2627-3106
Salma Lasram Borj-Cedria Biotechnology Center, Laboratory of Molecular Physiology of Plants, BP901, Hammam-Lif 2050, Tunisia https://orcid.org/0000-0003-2257-7743
Majdi Hammami Borj-Cedria Biotechnology Center, Laboratory of Aromatic and Medicinal Plants, BP901, Hammam-Lif 2050, Tunisia https://orcid.org/0000-0002-4376-0638
Walid Yeddes Borj-Cedria Biotechnology Center, Laboratory of Aromatic and Medicinal Plants, BP901, Hammam-Lif 2050, Tunisia https://orcid.org/0000-0002-1439-7956
Wissem Aidi Wannes Borj-Cedria Biotechnology Center, Laboratory of Aromatic and Medicinal Plants, BP901, Hammam-Lif 2050, Tunisia https://orcid.org/0000-0003-3134-0457
Saber Khammassi Borj-Cedria Biotechnology Center, Laboratory of Aromatic and Medicinal Plants, BP901, Hammam-Lif 2050, Tunisia https://orcid.org/0000-0003-3223-906X
Bouzid Nasraoui Carthage University, INAT, LR / Bioaggressors and Integrated Pest Management in Agriculture, LR14AGR02, Tunis, Tunisia https://orcid.org/0000-0002-1500-3701
Moufida Saidani Tounsi Borj-Cedria Biotechnology Center, Laboratory of Aromatic and Medicinal Plants, BP901, Hammam-Lif 2050, Tunisia https://orcid.org/0000-0001-6052-1367
Nehla Labidi Ben Hmida Borj-Cedria Biotechnology Center, Laboratory of Aromatic and Medicinal Plants, BP901, Hammam-Lif 2050, Tunisia https://orcid.org/0000-0002-7217-3475

DOI:

https://doi.org/10.29228/ijpbp.4

Keywords:

Alternaria alternata, Antifungal activity, Essential oils

Abstract

The leaf essential oil yields of clementine, cypress, rosemary, tea, and thyme were 0.22, 0.87, 1.46, 1.20, and 0.72%, respectively, based on the dry weight of the plant material. The leaf essential oils of rosemary, tea, and thyme contained the highest levels of oxygenated monoterpenes (60.14-91.70%). Rosemary and tea leaf essential oils were rich in 1,8-cineole (49.98% and 57.55%, respectively), and they have potent antifungal activity against Alternaria alternata strain (MIC = 5000 μg/ml). Thyme was rich in carvacrol (78.54%) and had a MIC of 6000 μg/ml against A. alternata strain. Clementine leaf essential oil was characterized by the predominance of monoterpene hydrocarbons (88.65%), and it possessed a weak antifungal activity against A. alternata (MIC = 8000 μg/ml). Cypress leaf essential oil was characterized by the predominance of oxygenated sesquiterpenes (60.67%), having an antifungal activity of 8000 μg/ml.

References

Adams, S., Kunz, B., Weidenbörner, M., 1996. Mycelial deformations of Cladosporium herbarum due to the application of eugenol or carvacrol. Journal of Essential Oil Research, 8(5), 535-540.

Alves, F.M.F., França, K.R.S., de Araújo, I.G., da Nóbrega, L.P., Xavier A.L.S., Lima T.S., Rodrigues, A.P.M.S., Júnior, A.F.M., Cardoso, T.A.L., 2019. Control of Alternaria alternata using Melaleuca essential oil (Melaleuca alternifolia). Journal of Experimental Agriculture International, 40(3), 1-10.

Amri, I., Hamrouni, L., Hanana, M., Gargouri, S., Jamoussi, B., 2013. Chemical composition, bio-herbicidal and antifungal activities of essential oils isolated from Tunisian common cypress (Cupressus sempervirens L.). Journal of Medicinal Plants Research, 7(16), 1070-1080.

Angioni, A., Barra, A., Cereti, E., Barile, D., Coïsson, J.D., Arlorio, M., Cabras, P., 2004. Chemical composition, plant genetic differences, antimicrobial and antifungal activity investigation of the essential oil of Rosmarinus officinalis L. Journal of Agricultural and Food Chemistry, 52(11), 3530-3535.

Aslam, M.F., Irshad, G., Naz, F., Khan, M.A., 2022. Evaluation of the antifungal activity of essential oils against Alternaria alternata causing fruit rot of Eriobotrya japonica. Turkish Journal of Biochemistry, https://doi.org/10.1515/tjb-2021-0225.

Bassolé, I.H.N., Lamien-Meda, A., Bayala, B., Tirogo, S., Franz, C., Novak, J., Dicko, M.H., 2010. Composition and antimicrobial activities of Lippia multiflora Moldenke, Mentha x piperita L. and Ocimum basilicum L. essential oils and their major monoterpene alcohols alone and in combination. Molecules, 15(11), 7825-7839.

Bhavaniramya, S., Vishnupriya, S., Al-Aboody, M.S., Vijayakumar, R., Baskaran, D., 2019. Role of essential oils in food safety: Antimicrobial and antioxidant applications. Grain & Oil Science and Technology, 2(2), 49-55.

Boukhris, M., Regane, G., Yangui, T., Sayadi, S., Bouaziz, M., 2012. Chemical composition and biological potential of essential oil from Tunisian Cupressus sempervirens L. Journal of Arid Land Studies, 22(1), 329-332.

Carson, C.F., Hammer, K.A., Riley, T.V., 2006. Melaleuca alternifolia (tea tree) oil: a review of antimicrobial and other medicinal properties. Clinical Microbiology Reviews, 19(1), 50-62.

Celiktas, O.Y., Kocabas, E.H., Bedir, E., Sukan, F.V., Ozek, 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.

Chouhan, S., Sharma, K., Guleria, S., 2017. Antimicrobial activity of some essential oils—present status and future perspectives. Medicines, 4(3), 58.

D’agostino, M., Tesse, N., Frippiat, J.P., Machouart, M., Debourgogne, A., 2019. Essential oils and their natural active compounds presenting antifungal properties. Molecules, 24(20), 3713.

Dube, J.P., 2014. Characterization of Alternaria alternata isolates causing brown spot of potatoes in South Africa (Master Thesis in Science (Agriculture) Plant Pathology). University of Pretoria. (accessed 2014 February).

Dugo, G., Cotroneo, A., Bonaccorsi, I., Trozzi, A., 2011. Composition of the volatile fraction of citrus peel oils, Chapter 1, 1–161; Dugo, G., Cotroneo, A., Bonaccorsi, I. Composition of petitgrain oils, Chapter 5, 253-331. In citrus oils: Composition, advanced analytical techniques, contaminants, and biological activity. Edits. Dugo, Mondello, L., CRC Press - Taylor & Francis Group, Bacon Raton.

Elansary, H.O., Salem, M.Z., Ashmawy, N.A., Yacout, M.M., 2012. Chemical composition, antibacterial and antioxidant activities of leaves essential oils from Syzygium cumini L., Cupressus sempervirens L. and Lantana camara L. from Egypt. Journal of Agricultural Science, 4(10), 144-152.

Elshafie, H.S., Camele, I., 2017. An overview of the biological effects of some mediterranean essential oils on human health. BioMed Research International, 2017, 9268468.

Germanà, M.A., Palazzolo, E., Chiancone, B., Saiano, F., 2013. Characterization of leaf essential oil composition of homozygous and heterozygous Citrus clementina Hort. Extan. and its Ancestors. Journal of Essential Oil Bearing Plants, 16(1), 92-101.

Golab, M., Skwarlo-Sonta, K., 2007. Mechanisms involved in the anti-inflammatory action of inhaled tea tree oil in mice. Experimental Biology and Medicine, 232(3), 420-426.

González, M.J., Marioli, J.M., 2010. Antibacterial activity of water extracts and essential oils of various aromatic plants against Paenibacillus larvae, the causative agent of American Foulbrood. Journal of Invertebrate Pathology, 104(3), 209-213.

Grati Affes, T., Chenenaoui, S., Zemni, H., Hammami, M., Bachkouel, S., Aidi Wannes, W., Lasram, S., 2022. Biological control of Citrus brown spot pathogen,“Alternaria alternata” by different essential oils. International Journal of Environmental Health Research, 1-14.

Guetat, A., Al-Ghamdi, F.A., Osman, A.K., 2014. 1, 8-Cineole, α-Pinene and Verbenone chemotype of essential oil of species Rosmarinus officinalis L. from Saudi Arabia. International Journal of Herbal Medicine, 2, 137-141.

Hamdani, F.Z., Allem, R., 2015. Antifungal activity of the leaf essential oil of citrus against Alternaria alternata in vivo. International Journal of Applied and Natural Sciences, 4(4), 15-24.

Hosni, K., Hassen, I., M’Rabet, Y., Casabianca, H., 2019. Biochemical response of Cupressus sempervirens to cement dust: Yields and chemical composition of its essential oil. Arabian Journal of Chemistry, 12(7), 1308-1314.

Joshi, A., Prakash, O., Pant, A.K., Kumar, R., Szczepaniak, L., Kucharska-Ambrożej, K., 2022. Methyl eugenol, 1, 8-cineole and nerolidol rich essential oils with their biological activities from three melaleuca species growing in Tarai region of North India. Brazilian Archives of Biology and Technology, 64, e21210186.

Kasali, A.A., Lawal, O.A., Eshilokun, A.O., Olaniyan, A.A., Opoku, A.R., Setzer, W.N., 2011. Citrus essential oil of Nigeria part V: Volatile constituents of sweet orange leaf oil (Citrus sinensis). Natural Product Communications, 6(6), 875-878.

Khadidja, M., Nassima, B., Chahrazed, B., Xavier, F., 2010. Chemical composition and antimicrobial activity of essential oils isolated from Algerian Juniperus phoenicea L. and Cupressus sempervirens L. Journal of Medicinal Plants Research, 4(10), 959-964.

Kowalczyk, A., Przychodna, M., Sopata, S., Bodalska, A., Fecka, I., 2020. Thymol and thyme essential oil—new insights into selected therapeutic applications. Molecules, 25(18), 4125.

Lakušić, D.V., Ristić, M.S., Slavkovska, V.N., Šinžar‐Sekulić, J.B., Lakušić, B.S., 2012. Environment‐Related Variations of the Composition of the Essential Oils of Rosemary (Rosmarinus officinalis L.) in the Balkan Penninsula. Chemistry & Biodiversity, 9(7), 1286-1302.

Lopez-Reyes, J.G., Spadaro, D., Preile, 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.

Mata, A.T., Proença, C., Ferreira, A.R., Serralheiro, M.L M., Nogueira, J.M.F., Araújo, M.E.M., 2007. Antioxidant and antiacetylcholinesterase activities of five plants used as Portuguese food spices. Food Chemistry, 103(3), 778-786.

Matasyoh, J.C., Kiplimo, J.J., Karubiu, N.M., Hailstorks, T.P., 2007. Chemical composition and antimicrobial activity of the essential oil of Satureja biflora (Lamiaceae). Bulletin of the Chemical Society of Ethiopia, 21(2), 249-254.

Mohammadi, A., Bahramikia, S., 2019. Molecular identification and genetic variation of Alternaria species isolated from tomatoes using ITS1 sequencing and inter simple sequence repeat methods. Current Medical Mycology, 5(2), 1-8.

Moore, J., Yousef, M., Tsiani, E., 2016. Anticancer effects of rosemary (Rosmarinus officinalis L.) extract and rosemary extract polyphenols. Nutrients, 8(11), 731.

Napoli, E.M., Curcuruto, G., Ruberto, G., 2010. Screening of the essential oil composition of wild Sicilian rosemary. Biochemical Systematics and Ecology, 38(4), 659-670.

Özcan, M.M., Chalchat, J.C., 2008. Chemical composition and antifungal activity of rosemary (Rosmarinus officinalis L.) oil from Turkey. International Journal of Food Sciences and Nutrition, 59(7-8), 691-698.

Padalia, R.C., Verma, R.S., Chauhan, A., Chanotiya, C.S., 2015. The essential oil composition of Melaleuca leucadendra L. grown in India: A novel source of (E)-nerolidol. Industrial Crops and Products, 69, 224-227.

Papageorgiou, V., Gardeli, C., Mallouchos, A., Papaioannou, M., Komaitis, M., 2008. Variation of the chemical profile and antioxidant behavior of Rosmarinus officinalis L. and Salvia fruticosa Miller grown in Greece. Journal of Agricultural and Food Chemistry, 56(16), 7254-7264.

Park, H.M., Kim, J., Chang, K.S., Kim, B.S., Yang, Y.J., Kim, G.H., Park, I.K., 2011. Larvicidal activity of Myrtaceae essential oils and their components against Aedes aegypti, acute toxicity on Daphnia magna, and aqueous residue. Journal of Medical Entomology, 48(2), 405-410.

Porte, A., Godoy, R.L., 2008. Chemical composition of Thymus vulgaris L.(Thyme) essential oil from the Rio de Janeiro state, Brazil. Journal of the Serbian Chemical Society, 73(3), 307-310.

Raveau, R., Fontaine, J., Lounès-Hadj Sahraoui, A., 2020. Essential oils as potential alternative biocontrol products against plant pathogens and weeds: A review. Foods, 9(3), 365.

Reiling, K.K., Yoshikuni, Y., Martin, V.J., Newman, J., Bohlmann, J., Keasling, J.D., 2004. Mono and diterpene production in Escherichia coli. Biotechnology and Bioengineering, 87(2), 200-212.

Sadeh, D., Nitzan, N., Chaimovitsh, D., Shachter, A., Ghanim, M., Dudai, N., 2019. Interactive effects of genotype, seasonality and extraction method on chemical compositions and yield of essential oil from rosemary (Rosmarinus officinalis L.). Industrial Crops and Products, 138, 111419.

Shaban, W., 2014. Evaluation of some fungicide alternatives against Alternaria fruit rot on tomato. Egyptian Journal of Phytopathology, 42(2), 91-104.

Shabnum, S., Wagay, M.G., 2011. Essential oil composition of Thymus vulgaris L. and their uses. Journal of Research and Development, 11, 83-94.

Silva, M.R., Ximenes, R.M., da Costa, J.G.M., Leal, L.K.A.M., de Lopes, A.A., de Barros Viana, G.S., 2010. Comparative anticonvulsant activities of the essential oils (EOs) from Cymbopogon winterianus Jowitt and Cymbopogon citratus (DC) Stapf. in mice. Naunyn-Schmiedeberg's Archives of Pharmacology, 381(5), 415-426.

Soković, M.D., Vukojević, J., Marin, P.D., Brkić, D.D., Vajs, V., Van Griensven, L.J., 2009. Chemical composition of essential oils of Thymus and Mentha species and their antifungal activities. Molecules, 14(1), 238-249.

Thi Nguyen, T.T., Thi Tran, T.T., Hua, T.M., Diep, T.T., Chau, D.K.N., Duus, F., Le, T.N., 2016. Investigation of peel and leaf essential oils of Citrus clementina Hort. ex Tan. growing in the south of Vietnam. Journal of Essential Oil Research, 28(2), 96-103.

Varela, F., Navarrete, P., Cristobal, R., Fanlo, M., Melero, R., Sotomayor, J.A., Cases, A., 2007. Variability in the chemical composition of wild Rosmarinus officinalis L. In I International Medicinal and Aromatic Plants Conference on Culinary Herbs, 826, 167-174.

Yan, R., Yang, Y., Zeng, Y., Zou, G., 2009. Cytotoxicity and antibacterial activity of Lindera strychnifolia essential oils and extracts. Journal of Ethnopharmacology, 121(3), 451-455.

Yeddes, W., Aidi Wannes, W., Hammami, M., Smida, M., Chebbi, A., Marzouk, B., Saidani Tounsi, M., 2018. Effect of environmental conditions on the chemical composition and antioxidant activity of essential oils from Rosmarinus officinalis L. growing wild in Tunisia. Journal of Essential Oil Bearing Plants, 21(4), 972-986.

Yeddes, W., Hammami, M., Khammassi, S., Grati Affes, T., Aidi Wannes, W., Saidani-Tounsi, M., 2022a. Antibacterial activities of rosemary (Rosmarinus officinalis L.) essential oil andethanol extract. Open Access Research Journal of Multidisciplinary Studies, 3(1), 1-8.

Yeddes, W., Mejri, I., Grati Affes, T., Khammassi, S., Hammami, M., Aidi-Wannes, W., Saidani Tounsi, M., 2022b. Combined effect of essential oils from Clove (Syzygium aromaticum (L.) Merr. & LM Perry), Thyme (Thymus vulgaris L.) and Lemon peel (Citrus limon (L.) Osbeck) on anti-bacterial, cytotoxic and anti-inflammatory activities. Trends in Phytochemical Research, 6(1), 11-18.

Zaouali, Y., Boussaid, M., 2008. Isozyme markers and volatiles in Tunisian Rosmarinus officinalis L.(Lamiaceae): A comparative analysis of population structure. Biochemical Systematics and Ecology, 36(1), 11-21.

Zerigui, F., Mouzaoui, F., 2018.Contribution à l’étude d’Alternaria sp., agent causal de l’alternariose de la pomme de terre : Prospection, isolement et identification du pathogène. Master research, Abdelhamid Ben Badis-Mostagane Univresity, Algeria, 49pp.