Diyala Agricultural Sciences Journal 2022, Vol (14) No 2: 24-32 ISSN: 2073-9524 eISSN: 2310-8746 24 Effectiveness of Essential Oils from Three Medicinal Plants Against Bayoud Disease (Fusarium oxysporum f. sp. albedinis) of Date Palm (Phoenix dactylifera L.) Boualem Boumaaza 1 , Abdelhamid Gacemi 2 , M’hamed Benada 3 , Sofiane Boudalia 4 , Ibrahim E. Benzohra 5 , Hakima Belaidi 6 , Omar Khaladi 7 1 University of Ibn khaldoun Tiaret. BP 78 zaâroura 14000, Tiaret, Algéria. 2 INRA Station de Recherche Hmadna. BP 48017 Relizane, Algéria. 3 University of Ahmed zabana. BP 48000 Bormadia Relizane, Algéria. 4 Laboratory of Biology, Water and Environment (LBEE), University of 8th May, 1945 Guelma, BP 401 24000 Guelma, Algeria. 5 Scientific and Technical Research Center on Arid Regions (CRSTRA) BP. Box 1682 RP 07000, Biskra, Algeria. Conservation Laboratory Wetlands. 6 Laboratoire Ecodéveloppement des Espaces, Department of Environmental Sciences, Djilali Liabes University of Sidi Bel Abbes, 22000 Sidi Bel Abbes, Algeria. 7 Laboratory of Biology, Water and Environment (LBEE), University of 8th May, 1945 Guelma, BP 401 24000 Guelma, Algeria. 1 Corresponding author: agroboum@hotmail.fr Article history: Received: 16 July 2022 Accepted: 17 August 2022 Published: 30 December 2022 Abstract Plant extracts and essential oils are promising new sources of non-toxic alternatives to chemicals substances. They are used for their antimicrobial properties against plant diseases of fungal origin, against bacterial, and those of virus origin. This study was carried out to study the antifungal activity of Artemisia herba-alba, Foeniculum vulgare and Citrus sinensis essential oils against Fusarium oxysporum f. sp. albedinis. Essential oil was extracted by steam distillation. Antifungal activity of essential oil was investigated by macro-broth method of dilution by a minimal inhibitory concentration (MIC) assay against this pathogen. The yield of essential oil obtained by steam distillation of Foeniculum vulgare samples was 2.31% greater than that obtained from Citrus sinensis sample which was 1.8%, followed by Artemisia herba alba samples 1.22%. Regarding antifungal activity, the results revealed a better inhibitory activity of Artemisia herba alba against the tested strainsat the lowest LC50 values (0.1 µl/ml). On the other hand, Foeniculum vulgare, Artemisia herba alba and Citrus sinensis essential oils show similar MICs of mycelial growth against this pathogen. The value of the MIC and CMF is greater than 50 µl/ml for the three essential oils. Keywords: Antimicrobial activity, biocontrol, essential oil, Fusarium oxysporum f. sp. albedinis, medicinal plant. https://dx.doi.org/10.52951/dasj.22142003 This article is open-access under the CC BY 4.0 license (http://creativecommons.org/licenses/by/4.0/). Introduction The date palm (Phoenix dactylifera L.) is considered one of the main perennial crops in the oasis ecosystem of several countries around the world (Fernández- López et al., 2022). The date palm is, first of all, a fruit tree and therefore the origin of a foodstuff, the date, which is fundamental for Saharan agricultural societies. It represents an ecological importance in the control against desertification (Jonoobi et al., 2019). The Algerian date palm sector has been showing signs of crisis for decades, with a duality between a traditional system that is not very competitive due to geomorphological conditions (in the Sahara zones) and a modern system, intended mainly for export. Despite this importance, the date palm has suffered from a major biotic constraint mailto:agroboum@hotmail.fr http://creativecommons.org/licenses/by/4.0/ https://orcid.org/0000-0003-0993-2931 https://orcid.org/0000-0001-9161-3504 https://orcid.org/0000-0002-6319-8822 https://orcid.org/0000-0002-7729-185X https://orcid.org/0000-0002-4234-9302 https://orcid.org/0000-0003-0809-1472 https://orcid.org/0000-0002-2861-0295 https://orcid.org/0000-0003-0993-2931 https://orcid.org/0000-0001-9161-3504 https://orcid.org/0000-0002-6319-8822 https://orcid.org/0000-0002-7729-185X https://orcid.org/0000-0002-4234-9302 https://orcid.org/0000-0003-0809-1472 https://orcid.org/0000-0002-2861-0295 https://orcid.org/0000-0003-0993-2931 https://orcid.org/0000-0001-9161-3504 https://orcid.org/0000-0002-6319-8822 https://orcid.org/0000-0002-7729-185X https://orcid.org/0000-0002-4234-9302 https://orcid.org/0000-0003-0809-1472 https://orcid.org/0000-0002-2861-0295 https://orcid.org/0000-0003-0993-2931 https://orcid.org/0000-0001-9161-3504 https://orcid.org/0000-0002-6319-8822 https://orcid.org/0000-0002-7729-185X https://orcid.org/0000-0002-4234-9302 https://orcid.org/0000-0003-0809-1472 https://orcid.org/0000-0002-2861-0295 https://orcid.org/0000-0003-0993-2931 https://orcid.org/0000-0001-9161-3504 https://orcid.org/0000-0002-6319-8822 https://orcid.org/0000-0002-7729-185X https://orcid.org/0000-0002-4234-9302 https://orcid.org/0000-0003-0809-1472 https://orcid.org/0000-0002-2861-0295 https://orcid.org/0000-0003-0993-2931 https://orcid.org/0000-0001-9161-3504 https://orcid.org/0000-0002-6319-8822 https://orcid.org/0000-0002-7729-185X https://orcid.org/0000-0002-4234-9302 https://orcid.org/0000-0003-0809-1472 https://orcid.org/0000-0002-2861-0295 https://orcid.org/0000-0003-0993-2931 https://orcid.org/0000-0001-9161-3504 https://orcid.org/0000-0002-6319-8822 https://orcid.org/0000-0002-7729-185X https://orcid.org/0000-0002-4234-9302 https://orcid.org/0000-0003-0809-1472 https://orcid.org/0000-0002-2861-0295 Diyala Agricultural Sciences Journal 2022, Vol (14) No 2: 24-32 25 called, Bayoud, in Algeria, Mauritania and Morocco (Bouguedoura et al., 2015). Bayoud is a destructive and fatal vascular disease caused by the soil fungus Fusarium oxysporum f. sp. albedinis (Foa) (Benzohra et al., 2017). The fungus lives in the soil and attacks palm trees of all ages through the roots. After a period the heart of the tree ends up giving way causing its death. This disease has killed in the last fifty years more than 10 million palm trees in Morocco and three million in Algeria (Bouguedoura et al., 2015). Efforts to control this epidemic have focused on several methods such as prophylactic measures, varietal selection and biological control, in order to limit the damage caused by this epidemic. In addition to these measures, the control against the bayoud agent has been highlighted in previous works (Belaidi, 2022a; Belaidi, 2022b). Due to the problems caused by chemical substances, the development of alternative control measures is of great importance. Biological control has been considered as a desirable and realistic alternative. Numerous studies have demonstrated the ability of several essential oils to possess antibacterial, antifungal, antiviral, antioxidant activities and play an important role in the protection of the plants and the human body against plant pathogens both in vitro and in vivo (Mutlu-Ingoket al., 2020; Marin-Tinoco et al., 2021). Note that essential oils can be an effective solution, as their toxicity is much lower, better specificity of action, biodegradable and environmentally friendly (Campos et al., 2019). It has been reported that essential oils possess various actions on pathogenic fungi, such as disruption of the cytoplasmic membrane, disruption of the proton driving force, electron leakage and coagulation of the protein content of cells, acidification from inside the cell, blocking the production of cellular energy and the synthesis of structural components. The essential oil may inhibit the cell growth and proliferation by interrupting ergosterol biosynthesis (Gao et al., 2016). Essential oil enables us to integrate into the lipids of the cell membrane, increasing permeability occur as a due of loss of ions and reduction of membrane potential, collapse of the proton pump and depletion of the ATP pool, which eventually lead to leaking of intracellular constituents, coagulation of cell contents, lysis and cell death (Turgis et al., 2012). The aim of this research is to evaluate the antifungal activity of extracts (natural substances) of three locally available plants against Fusarium oxysporum f. sp. albedinis. Materials and Methods Inoculum preparation The tested Fusarium oxysporum f. sp. albedinis strain B7b7245 was preserved at the Bioresources Laboratory of the Center for Scientific and Technical Research on Arid Regions, Biskra, Algeria. Fusarium oxysporum f. sp. albedinis readily produced conidia after 14 days on potato dextrose agar (PDA; potato dextrose agar.SPA CRAPC Algeria) plate at 25∘C in the dark. Conidial suspension was obtained by flooding plates with distilled water and rubbing gently with a glass rod, then filtered through sterile cheesecloth. The conidia concentration present in the initial suspension (adjusted to the concentration 1 × 10 5 conidia.mL -1 ) was quantified using the hemocytometer. Extraction of essential oils The essential oils were extracted from the dry leaves and seeds by steam distillation carried out in a still system (Machado et al., 2022). The plant material was placed in a pressure cooker that was connected to a cooler through a conduit. The whole (pressure cooker, leaves and water separated by a grid) was brought to the boil on an electric stove. Water vapor and condensed aromatic molecules were collected in a separatory funnel. The supernatant oils were recovered by decantation and stored in opaque bottles. Diyala Agricultural Sciences Journal 2022, Vol (14) No 2: 24-32 26 Essential oils yield (%) The yield (%, w/w) from plants was calculated as: R (%) = mH . l00/mS. Growth inhibition evaluation Evaluation the growth inhibition of Fusarium oxysporum f. sp. albedinis strains, was calculated by the following equation Mohareb el al. (2017): L (%) = [(D1 – D2)/D1] × 100 Where: L (%): Rate of mycelial growth inhibition D1: Mycelial growth in control D2: Mycelial growth in the presence of treatment. In vitro antifungal assay Antifungal activity of the essential oil against Fusarium oxysporum f. sp. albedinis was investigated by macro-broth method of dilution (Balouiri et al., 2016).Then, 100 μl of the essential oil was poured into the plates. Mycelium growth inhibition was evaluated by placing 30 μl of the inoculum containing 10 5 spores.mL -1 in the centre of a PDA plate. Cultures were incubated at 25∘C in the dark. Colony diameters were measured in two perpendicular directions, after 24 hours and again after 96 hours. Each treatment had five replications. In the control group, the oil was replaced by sterile distilled water. Statistical analysis All data were analyzed using ANOVA test. A Comparison of means was performed by test of Kruskal-Wallis at 5% of probability. The software used was STATBOX 6.0.4. Results and Discussion Essential oils yield (%) The average essential oil yields were estimated using the plant material. The rate obtained from Foeniculum vulgare samples was 2.31% greater than that obtained from Citrus sinensis sample which was 1.8%, followed by Artemisia herba alba samples 1.22% (Table 1). This rate is low when compared to that obtained from Foeniculum vulgare from Iran and Turkey, which is 3.77 and 2.67% respectively (Sabzi- Nojadeh et al., 2021). In addition, the essential oil yields for Citrus sinensis fresh fruits reported in this study are similar to those reported by Bhandari et al. (2021). For the Artemisia herba alba species, our yield is higher compared to Artemisia herba alba provenances in Morocco (1.18%) (Allali et al., 2022). In Tunisia, the same infraspecific variance in Artemisia herba alba yield was varied between 0.68% and 1.93% based on dried weight of samples (Mohsen and Ali, 2009). Plant species, environmental conditions, extraction technique, drying, and cultivation practices, are all aspects that influence the yield, content and chemical composition of essential oils (Rezouki et al., 2021). Table 1. Essential oils yield (%) and groups of compounds, region of collection Species Essential oils yield (%) Previous studies on the majority compounds (References) Artemisia herba alba 1.22 Camphor : Algeria (Lakehal et al., 2016) α-Thujone : Tunisia (Mohsen and Ali, 2009); Morroco (Bencheqroun et al., 2012 ) 1,8-cineole Spain (Mohamed et al., 2010) Verbenol : Morroco (Tilaoui et al., 2011) Diyala Agricultural Sciences Journal 2022, Vol (14) No 2: 24-32 27 Citrus sinensis 1.8 Flavonoids: Florida (Abbate et al., 2012) Limonene : Uganda (Njoroge et al., 2013 ; Kamal et al., 2011) Linalool ; Egypt (Tisserand et al., 2014) Foeniculum vulgare 2.3 Limonene: Morocco (El Ouariachi et al., 2014) Stigmasterol: Egypt (Nassar et al., 2010) trans-anethole: Slovakia (Petra et al., 2021 ) a-pinene : Iraq (Belaidi et al., 2020 ) Activity of essential oil on mycelial growth Artemisia herba alba essential oil was evaluated at concentrations of 0.1, 1, 10, 30, and 50 µl.ml -1 , which resulted in inhibition rates of 51.9, 61.5, 76.2, 76.4, and 82.6%, respectively (Table 2). Indeed, the concentration equal to or greater than 0.1 µl.ml -1 of essential oil inhibits 50% the growth of Fusarium oxysporum f. sp albedinis. Fusarium oxysporum f. sp. albedinis's growth is inhibited by 50% at concentrations equivalent to or greater than 0.1 µl.ml -1 . In terms of kinetics of action, 24 hours of treatment is enough to limit 50% mycelial growth. Similarly, Janaćković et al. (2015) shown that Artemisia herba alba essential oil showed better antifungal activities against eight fungal species; A.niger A. ochraceus, A. versicolor, A. fumigatus, Penicillium ochrochloron, P. funiculosum, Trichodermaviride and Candida albicans. According to earlier results, oxygenated monoterpenes, particularly thujone, have a stronger antifungal potential (Sokovi et al., 2010). Table 2. Antifungal activity of Artemisia herbaalbaessential oïl against fungal strain. Values are the means of the inhibition rates ± SD Time Essential oïl concentrations (µl.ml -1 ) 0.1 1 10 30 50 1st day 54.7±4.2 58.1±3.6 62.8±6.4 73.6±3.7 77.6±1.7 2nd day 40.4±5 50.5±10.3 65.4±4.5 76.3±2.17 78.1±1.44 3rd day 47.9±2.3 59.5±4.92 72.1±4.6 79.2±1.7 81.2±2.2 4th day 51.9±3.3 61.5±4.8 76.2±4.0 76.4±1.8 82.6±3.81 The results of antifungal activity assays showed that the 0.1,1, 10, 30 and 5 µl.ml - 1 Foeniculum vulgare essential oil produce an inhibition of 35.9, 36.7, 37.5, 38.4 and 50.4% respectively the mycelium growth of Fusarium oxysporum f. sp. albedinis after 24 hours of incubation at 25∘C compared to untreated (Table 3). According to these results, fennel essential oil inhibits growth at a rate of more than 50% in Petri dishes containing 50µl.ml -1 concentrations of the oil. According to Garzoli et al. (2018), the essential oil of Foeniculum vulgare has an inhibitory effect on the growth of the genus Candida due to the higher constituents of estragole, limonene, and fenchone. Some authors have demonstrated that trans- anethole is the primary active ingredient responsible for fennel oil's antimicrobial activity (Petra et al., 2021). Diyala Agricultural Sciences Journal 2022, Vol (14) No 2: 24-32 28 Table 3. Antifungal activity of Foeniculum vulgare essential oïl against fungal strain. Values are the means of the inhibition rates ± SD Time Essential oïl concentrations (µl.ml -1 ) 0.1 1 10 30 50 1st day 50.1±12.7 54.5±3.6 55.6±4.8 55.5±2.8 61.4±3.4 2nd day 35.9±2.1 36.7±2.0 37.5±3.3 38.4±3.0 50.4±3.7 3rd day 35.5±3.8 36.6±1.5 40.9±5.8 42.7±3.1 45.2±2.3 4th day 37.9±3.6 44.2±6.6 47.9±5.1 48.7±2.5 50.1±2.8 The Citrus sinensis essential oil reached the inhibition rate of 23.3, 25.9, 28.4, 28.4 and 34.6% for concentrations 0.1, 1, 10, 30 and 50 µl.ml -1 , respectively (Table 4). In fact, citrus essential oils did, have a very weak activity when applied to the tested strain of Fusarium oxysporum f. sp. albedinis. Sweet C. lemon, C. aurantifolia, C. maxima, and Citrus sinensis essential oil were reported to inhibit the growth of several fungal species, such as fungal species, such as R.solani, S.rolfsii, F.solani, F.oxysporum, F.semtectium, B.cinerea, and A. alternate (Sedeek et al., 2021). Their high content of monoterpenes, particularly limonene, may be responsible for their powerful antifungal effect (Singh et al., 2010). Table 4. Antifungal activity of Citrus sinensis essential oïl against fungal strain. Values are the means of the inhibition rates ± SD Time Essential oïl concentrations (µl.ml -1 ) 0.1 1 10 30 50 1st day 50.1±5.4 60.9±2.8 61.8±4.8 64.1±3.3 64.9±2.2 2nd day 40.3±4.0 44.9±5.3 53.01±3.1 52.9±1.3 53.4±1.7 3rd day 35.8±6.3 38.2±0.7 38.2±4.1 42.4±5.9 56.5±3.9 4th day 23.3±5.5 25.9±3.6 28.4±4.7 28.4±8.03 34.6±4.6 Comparison between the activities of different EOs on the mycelial growth of Fusarium oxysporum f. sp. albedinis The minimum inhibitory concentration (MIC) of essential oils was determined according to the method cited by Mizanur- Rahman et al. (2017). The comparison between the activities of the different essential oils against Fusarium oxysporum f. sp. albedinis, shows that Artemisia herba alba essential oil has a better inhibitory activity of mycelial growth. On the other hand, Foeniculum vulgare, Artemisia herba alba and Citrus sinensis essential oils show similar MICs of mycelial growth against this pathogen (Table 5). Table 5. Comparison of the Antifungal activity of A. herba alba, Foeniculum vulgare and Citrus sinensis essential oils against fungal strain.Values are the means of the inhibition rates ± SD Essential oils Essential oïl concentrations µl/ml 0.1 1 10 30 50 A. herba alba 51,9±6.2 61,5±8.3 76,2±7.4 76,4±7.7 82,6±11.2 F. vulgare 37,9±3.8 44,2±4.4 47,9±1.9 48,7±2.1 50,1±2.3 C. sinensis 23,3±4.2 25,9±1.2 28,4±1.2 28,4±1.5 34,6±2.01 The value of the MIC and MFC is greater than 50 µl/ml for the three essential oils (Table 6). Previous studies showed that Artemisia herba alba essential oil showed fungicidal and Diyala Agricultural Sciences Journal 2022, Vol (14) No 2: 24-32 29 fungistatic effects against Candida albicans with MIC (31.25 µl/ml) and MFC (62.5 µl/ml) (Boukhennoufa et al., 2019). Perczak et al. (2019) showed that the essential oil of Foeniculum vulgare inhibited the growth of Fusarium culmorum and the minimum inhibitory concentration (MIC) was >100 µg/cm 3 . EOs from two medicinal plants (Citrus sinensis and C. limon) were investigated for their antifungal activity against A. flavus by Ben Miri et al. (2018), who reported that the MIC values were 1.75 mg.mL-1 for C. limon and 2 mg.mL-1 for C. sinensis. The MFC of Citrus limon and Citrus sinensis occurred at 2 mg.mL - 1 . Table 6. Comparison of the Minimum inhibitory concentration (MIC), legal (LC50) and minimum fungicidal concentrations (MFC) of essential oils against fungal strain Essential oils A. herba alba Foeniculum vulgare C. sinensis MIC ˃50 µl/ml ˃50 µl/ml or equal to double CL50 ˃50 µl/ml LC50 0.1 µl/ml 50 µl/ml ˃50 µl/ml MFC ˃50 µl/ml ˃50 µl/ml ˃50 µl/ml Artemisia herba alba was shown to be the most effective against fungal strain with LC50, values that were lower than those obtained with Foeniculum vulgare and Citrus sinensis essential oils (LC50=0.1 µl/ml). The lowest LC50 was obtained with Artemisia herba alba (0.1 µl/ml), while the highest was obtained with Foeniculum vulgare and Citrus sinensis essential oils (˃50 µl/ml). Theoretically, to produce the fungicidal action with Artemisia herba alba and Foeniculum vulgare essential oils, the LC50 must be at least doubled. Contrarily, with Citrus sinensis essential oil, triple the CL50 is sufficient to produce this effect (MFC). Conclusion In summary, the present work confirms the very important of Artemisia herba alba, Foeniculum vulgare and Citrus sinensis essential oils for their possible antifungal activity. Indeed; the agar diffusion method revealed that Artemisia herba-alba essential oil exhibited potent antifungal activity against Fusarium oxysporum f. sp. albedinis. In the same way the lowest LC50 was obtained with Artemisia herba alba (0.1 µl/ml), while the highest was obtained with Foeniculum vulgare and Citrus sinensis essential oils (˃50 µl/ml). 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