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In Vitro Antifungal Activity and Chemical Composition of Piper Auritum Kunth Essential Oil Against Fusarium Oxysporum and Fusarium Equiseti

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In Vitro Antifungal Activity and Chemical Composition of Piper Auritum Kunth Essential Oil Against Fusarium Oxysporum and Fusarium Equiseti agronomy Article In Vitro Antifungal Activity and Chemical Composition of Piper auritum Kunth Essential Oil against Fusarium oxysporum and Fusarium equiseti César Chacón 1 , Emanuel Bojórquez-Quintal 2 , Goretty Caamal-Chan 3,Víctor M. Ruíz-Valdiviezo 1 , Joaquín A. Montes-Molina 1, Eduardo R. Garrido-Ramírez 4 , Luis M. Rojas-Abarca 5 and Nancy Ruiz-Lau 6,* 1 Tecnológico Nacional de México/Instituto Tecnológico de Tuxtla Gutiérrez, Carretera Panamericana km. 1080, 29050 Tuxtla Gutiérrez, Chiapas, Mexico; [email protected] (C.C.); [email protected] (V.M.R.-V.); [email protected] (J.A.M.-M.) 2 CONACyT-Laboratorio de Análisis y Diagnóstico del Patrimonio, El Colegio de Michoacán. A.C., Cerro de Nahuatzen 85, Fracc, Jardines del Cerro Grande, 59370 La Piedad, Michoacán, Mexico; [email protected] 3 CONACyT-Centro de Investigaciones Biológicas del Noroeste, S.C. Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur, 23096 La Paz, Baja California Sur, Mexico; [email protected] 4 Campo Experimental Centro de Chiapas-INIFAP, Carretera Ocozocoautla-Cintalapa Km3, 29140 Ocozocoautla, Chiapas, Mexico; [email protected] 5 Laboratorio de Análisis y Diagnóstico del Patrimonio, El Colegio de Michoacán. A.C., Cerro de Nahuatzen 85, Fracc, Jardines del Cerro Grande, 59370 La Piedad, Michoacán, Mexico; [email protected] 6 CONACyT-Tecnológico Nacional de México/Instituto Tecnológico de Tuxtla Gutiérrez, Carretera Panamericana km. 1080, 29050 Tuxtla Gutiérrez, Chiapas, Mexico * Correspondence: [email protected]; Tel.: +52-9993605266 Citation: Chacón, C.; Bojórquez-Quintal, E.; Caamal-Chan, Abstract: The essential oils of plants of the genus Piper have secondary metabolites that have G.; Ruíz-Valdiviezo, V.M.; Montes- Molina, J.A.; Garrido-Ramírez, E.R.; antimicrobial activity related to their chemical composition. The objective of our work was to Rojas-Abarca, L.M.; Ruiz-Lau, N. In determine the chemical composition and evaluate the antifungal activity of the aerial part essential Vitro Antifungal Activity and oil of P. auritum obtained by hydrodistillation on Fusarium oxysporum and Fusarium equiseti isolated Chemical Composition of Piper from Capsicum chinense. The antifungal activity was evaluated by direct contact and poisoned food auritum Kunth Essential Oil against tests, and the minimum inhibitory concentration (MIC50) and maximum radial growth inhibition Fusarium oxysporum and Fusarium (MGI) were determined. The identification of oil metabolites was carried out by direct analysis in real equiseti. Agronomy 2021, 11, 1098. time mass spectrometry (DART-MS). By direct contact, the essential oil reached an inhibition of over https://doi.org/10.3390/ 40% on Fusarium spp. The 8.4 mg/mL concentration showed the highest inhibition on F. oxysporum agronomy11061098 (40–60%) and F. equiseti (>50%). The MIC50 was 6 mg/mL for F. oxysporum FCHA-T7 and 9 mg/mL for F. oxysporum FCHJ-T6 and F. equiseti FCHE-T8. DART-MS chemical analysis of the essential Received: 30 April 2021 oil showed [2M-H]− and [M-H]− adducts of high relative intensity that were mainly attributed to Accepted: 25 May 2021 eugenol and thymol/p-cimen-8-ol. The findings found in this study show a fungistatic effect of the Published: 28 May 2021 essential oil of P. auritum on Fusarium spp. Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in Keywords: aerial part; inhibition; fungistatic; metabolites; safrole; eugenol; thymol published maps and institutional affil- iations. 1. Introduction Diseases caused by pathogenic fungi transmitted by the soil constitute an important Copyright: © 2021 by the authors. limitation for the yield and quality of vegetable crops and fruit in intensive agriculture [1]. Licensee MDPI, Basel, Switzerland. Chili (Capsicum spp.) is a fruit and spice native to South and Central America [2], which This article is an open access article belongs to the Solanaceae family and is known for its flavor and pungency [3]. The genus distributed under the terms and Capsicum is made up of a group of herbaceous plants [4], of which five species (C. annuum, conditions of the Creative Commons C. baccatum, C. chinense, C. frutescens and C. pubescens) were domesticated and are currently Attribution (CC BY) license (https:// cultivated in different parts of the world [4,5]. Therefore, from an economic point of view, creativecommons.org/licenses/by/ it is one of the most important vegetables worldwide [4]. 4.0/). Agronomy 2021, 11, 1098. https://doi.org/10.3390/agronomy11061098 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, 1098 2 of 13 Fungal wilt, root rot, and charcoal rot are the most damaging diseases for plant crops, including those of the genus Capsicum [6]. Crown and root rots are by far the most widespread disease caused by Fusarium spp., and several species of Fusarium are recognized as causative agents [7]. Recent reports have reported F. oxysporum as a causative agent of chili root and basal stem rot [8], and most shoot vascular wilt is caused by this species [9]. Fusarium equiseti is a pathogenic species associated with leaf spot, root and crown rot, and fruit rot, which cause seed decomposition and seedling infection in different fruit and vegetable crops, as well as cereals and spices [10]. To combat microbial diseases, chemical control methods are applied that are irritating, toxic, mutagenic, teratogenic, and carcinogenic to users, as well as having serious ecologi- cal consequences. Synthetic chemicals provided promising results against wilt; however, fungicide application under field conditions involves environmental contamination, in- consistency in efficacy, and high costs [11]. The development of resistance of pathogenic fungi towards synthetic fungicides is of great concern. Therefore, it is important to develop safe, effective, and friendly fungicides with the environment and with the farmers and producers. This generates interest in alternative (green) sources of antifungal compounds that are more environmentally friendly, and that help reduce the intensive use of these products. Plants have, and continue to be, sources of antifungal compounds [12]. Many of these compounds have biological activity, are more degradable than many pesticides, and can significantly reduce the risk of adverse ecological effects [13]. Plant extracts are an alternative method to the use of chemical substances as a green treatment, since they have a wide variety of secondary metabolites that have demonstrated antimicrobial prop- erties [14]. Essential oils produced by aromatic plants are a complex mixture of volatile secondary metabolites [15] known for their natural components, such as monoterpenes, diterpenes, and hydrocarbons with various functional groups, which have been studied for their antifungal activities [16]. Piper is the largest genus of the Piperaceae family, which is distributed throughout the tropics, with significant concentrations in Central and South America, the Caribbean, Africa, Asia, and some Pacific islands. The aroma emitted by its leaves, fruits and roots has caused the species of this genus to be widely used as a flavoring ingredient in cuisine [17]. It is also used for its therapeutic properties in traditional medicine. The secondary metabolites in extracts from various parts of this plant have shown antifungal, insecticidal, antifeedant, bactericidal and cytotoxic activity [18]. Piper’s secondary compounds such as safrole, dilapiol, myristicin, and methylene- dioxyphenyl have been reported to have biological activity [18]. In the analysis of antifungal activity chemical compounds such as safrole and dillapiole obtained from essential oil of P. auritum and P. holtonii, respectively, have been reported to have a direct fungitoxic effect in vitro against Botryodiplodia theobromae and Colletotrichum acutatum, and it was found that the highest values of inhibition of mycelial growth of both fungi were obtained for dillapi- ole, compared to safrole [19]. There are reports that test different phytoextracts obtained from P. auritum on different phytopathogenic fungi, including the genus Fusarium. The es- sential oil of P. auritum has been tested against Alternaria solani, inhibiting mycelial growth at seven and fourteen days [20]. In another study, a total inhibition (fungicidal effect) of the mycelial growth of Curvularia lunata, Sarocladium oryzae and Bipolaris oryzae was reported at 96 h [21]. In a previous report, it was observed that the essential oil of P. auritum leaves had an inhibitory effect on the growth of F. oxysporum f. sp. comiteca (75.32%), F. oxysporum f. sp. tequilana (86.57%), and F. solani f. sp. comiteca (63.36%), indicating a fungistatic effect [22]. While in another report, the essential oil of P. auritum caused total inhibition of the growth of F. solani (F2 and F5 isolates) and of F. redolens (F3 isolates) [23]. The increase in food production, the regulations on the use of synthetic fungicides, the development of resistance in phytopathogens justify the search for other control alter- natives [6], as the phytochemical that together with an integrated management of the crop could be successful. Therefore, the objective of the present research was to determine the Agronomy 2021, 11, 1098 3 of 13 chemical composition and evaluate the antifungal activity of the essential oil of the aerial part of P. auritum on the species of F. oxysporum and F. equiseti causing the wilt in chili. 2. Materials and Methods 2.1. Plant Material and Essential Oil Leaves and inflorescences
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