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Chemical Characterization of Plant Extracts and Evaluation of Their Nematicidal and Phytotoxic Potential

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Chemical Characterization of Plant Extracts and Evaluation of Their Nematicidal and Phytotoxic Potential molecules Article Chemical Characterization of Plant Extracts and Evaluation of their Nematicidal and Phytotoxic Potential Raúl Velasco-Azorsa 1,Héctor Cruz-Santiago 2, Ignacio Cid del Prado-Vera 3, Marco Vinicio Ramirez-Mares 4, María del Rocío Gutiérrez-Ortiz 5, Norma Francenia Santos-Sánchez 2, Raúl Salas-Coronado 2, Claudia Villanueva-Cañongo 2, Karla Isabel Lira-de León 6 and Beatriz Hernández-Carlos 2,* 1 Instituto de Recursos, Universidad del Mar, Puerto Ángel, San Pedro Pochutla, Oaxaca 70902, Mexico; [email protected] 2 Instituto de Agroindustrias, Universidad Tecnológica de la Mixteca, Acatlima, Huajuapan de León, Oaxaca 69000, Mexico; [email protected] (H.C.-S.); [email protected] (N.F.S.-S.); [email protected] (R.S.-C.); [email protected] (C.V.-C.) 3 Colegio de Postgraduados, km 36.5 Carretera México-Texcoco, Montecillos, Estado de Mexico, Texcoco 56230, Mexico; [email protected] 4 Departamento de Ingeniería Química y Bioquímica, Tecnológico Nacional de México/I.T. Morelia, Av. Tecnológico 1500, Lomas de Santiaguito, Morelia 58120, Mexico; [email protected] 5 Instituto de Ecologia, Universidad del Mar, Puerto Ángel, San Pedro Pochutla, Oaxaca 70902, Mexico; Citation: Velasco-Azorsa, R.; [email protected] Cruz-Santiago, H.; Cid del 6 Facultad de Química, Universidad Autónoma de Querétaro, Las Campanas, Querétaro 76010, Mexico; Prado-Vera, I.; Ramirez-Mares, M.V.; [email protected] Gutiérrez-Ortiz, M.d.R.; * Correspondence: [email protected]; Tel.: +52-9535320399 Santos-Sánchez, N.F.; Salas-Coronado, R.; Villanueva-Cañongo, C.; Lira-de Abstract: Nacobbus aberrans ranks among the “top ten” plant-parasitic nematodes of phytosanitary León, K.I.; Hernández-Carlos, B. importance. It causes significant losses in commercial interest crops in America and is a potential risk Chemical Characterization of Plant in the European Union. The nematicidal and phytotoxic activities of seven plant extracts against N. Extracts and Evaluation of their aberrans and Solanum lycopersicum were evaluated in vitro, respectively. The chemical nature of three Nematicidal and Phytotoxic Potential. −1 nematicidal extracts (EC50,48h ≤ 113 µg mL ) was studied through NMR analysis. Plant extracts Molecules 2021, 26, 2216. showed nematicidal activity on second-stage juveniles (J2): (≥87%) at 1000 µg mL−1 after 72 h, and https://doi.org/10.3390/ their EC values were 71.4–468.1 and 31.5–299.8 µg mL−1 after 24 and 48 h, respectively. Extracts with molecules26082216 50 −1 the best nematicidal potential (EC50,48h < 113 µg mL ) were those from Adenophyllum aurantium, Academic Editors: Young Pyo Jang, Alloispermum integrifolium, and Tournefortia densiflora, which inhibited L. esculentum seed growth −1 Yuntao Dai and Luis by 100% at 20 µg mL . Stigmasterol (1), β-sitosterol (2), and α-terthienyl (3) were identified Francisco Salomé-Abarca from A. aurantium, while 1, 2, lutein (4), centaurin (5), patuletin-7-β-O-glucoside (6), pendulin (7), and penduletin (8) were identified from A. integrifolium. From T. densiflora extract, allantoin (9), Received: 1 March 2021 9-O-angeloyl-retronecine (10), and its N-oxide (11) were identified. The present research is the first Accepted: 9 April 2021 to report the effect of T. densiflora, A. integrifolium, and A. aurantium against N. aberrans and chemically Published: 12 April 2021 characterized nematicidal extracts that may provide alternative sources of botanical nematicides. Publisher’s Note: MDPI stays neutral Keywords: Nacobbus aberrans; nematicidal activity; α-terthienyl; stigmasterol; quercetagetin deriva- with regard to jurisdictional claims in tives; 9-O-angeloyl-retronecine N-oxide published maps and institutional affil- iations. 1. Introduction The plant parasite nematode, Nacobbus aberrans (Thorne, 1935; Thorne & Allen, 1994), Copyright: © 2021 by the authors. also known as false root-knot, is distributed in Argentina, Bolivia, Chile, Ecuador, Mexico, Licensee MDPI, Basel, Switzerland. Peru, and the USA. It reduces crop yield in tomatoes (Solanum lycopersicum L.), pota- This article is an open access article toes (Solanum tuberosum), beans (Phaseolus vulgaris L.), and sugar beets (Beta vulgaris). distributed under the terms and conditions of the Creative Commons The nematode ranks among the “top ten” plant-parasitic nematodes of phytosanitary Attribution (CC BY) license (https:// importance [1]. It is estimated it meets the criteria to be a potential risk in the EU [2]. creativecommons.org/licenses/by/ Management strategies of plant-parasitic nematodes are cultural practices (crop rotation), 4.0/). mixed-cropping, organic amendments, resistant crop cultivars, biological control [3–6], Molecules 2021, 26, 2216. https://doi.org/10.3390/molecules26082216 https://www.mdpi.com/journal/molecules Molecules 2021, 26, x FOR PEER REVIEW 2 of 13 Molecules 2021, 26,strategies 2216 of plant-parasitic nematodes are cultural practices (crop rotation), mixed-crop- 2 of 13 ping, organic amendments, resistant crop cultivars, biological control [3–6], chemical ne- maticides, and bioactive products of plant origin. Among these strategies, natural product usage representschemical a vital nematicides,option for controlling and bioactive phytopathogenic products of plant nematodes origin. because Among of these strategies, their low impactnatural on the product environment usage representsand non-ta arget vital organisms. option for controllingIn the search phytopathogenic for botanic nematodes nematicides, somebecause of the of most their recent low impact proposals on the are environment using Stevia andrebaudiana non-target and organisms.Origanum In the search vulgare to controlfor Meloidogyne botanic nematicides,; in vivo experiments some of the mostshowed recent this proposals effect [7,8]. are In using the caseStevia of rebaudiana and N. aberrans, crudeOriganum herbal extracts vulgare tofrom control T. lunulateMeloidogyne [9], Cosmos; in vivo sulphureusexperiments [6], Senecio showed salignus this effect [7,8]. In [6], Witheringiathe stramoniifolia case of N. [6], aberrans and Lantana, crude cámara herbal [6] extracts showed from in vitroT. lunulate nematicidal[9], Cosmos activ- sulphureus [6], ity at 500 µg mLSenecio−1 (>70%) salignus to second-stage[6], Witheringia juvenile stramoniifolia (J2) individuals.[6], and Simultaneously,Lantana cámara in [vivo6] showed in vitro − protection fromnematicidal infection of activity Lycopersicum at 500 esculentumµg mL 1 (>70%)Mill and to Capsicum second-stage annumm juvenile plants (J2) individuals. occurred with extractsSimultaneously, of Tagetesin erecta vivo [9]protection and Trichilia from galuca infection [10], respectively. of Lycopersicum There esculentum are Mill and only two reportsCapsicum of natural annumm compoundsplants occurredwith toxic with potential extracts for of theTagetes control erecta of [N.9] aberrans and Trichilia: galuca [10], capsidiol acts asrespectively. a nematostatic There on are N. onlyaberrans two J2 reports (90% immobility) of natural compounds at 1.5 µg mL with−1 after toxic 72 potential for the h [11]; and variouscontrol cadinenes of N. aberrans affect: immobility-mortality capsidiol acts as a nematostatic (LC50 25.4–111.4 on N. aberransµg mL−1)J2 and (90% immobility) −1 µ −1 inhibit eggs hatchingat 1.5 (ICg mL50 31.23–56.71after 72 µg h [mL11]; and) [12]. various Identification cadinenes of substances affect immobility-mortality from bo- (LC50 −1 −1 tanical origins 25.4–111.4capable ofµ controllingg mL ) and N. inhibit aberrans eggs lies hatching partially (IC on50 differences31.23–56.71 withµg mL other)[ 12]. Identifica- common plant-parasitiction of substances nematodes from (e.g., botanical Meloidogyne origins spp capable.), such of as controlling its endoparasiticN. aberrans stagelies partially on (migratory anddifferences sedentary), with several other infective common stages, plant-parasitic and 15–30 nematodesdays dehydration (e.g., Meloidogyne tolerance spp.), such as of J3 and J4 larvaeits endoparasitic [13]. This research stage (migratoryidentifies botanical and sedentary), sources several of compounds infective with stages, ne- and 15–30 days maticidal or nematostaticdehydration characteristics tolerance of J3by andscreening J4 larvae seven [13 ].plant This species research for identifies nematicidal botanical sources activities againstof N. compounds aberrans J2 with individuals nematicidal and phytotoxicity or nematostatic to tomato characteristics seeds. NMR by screening anal- seven plant species for nematicidal activities against N. aberrans J2 individuals and phytotoxicity to ysis established the chemical nature of nematicidal extracts (EC50,48h ≤ 112.3 µg mL−1) as sterol, thiophene,tomato flavonoid, seeds. and NMR alkaloid-l analysisike establishedcompounds the(Figure chemical 1). Some nature of these of nematicidal com- extracts ≤ µ −1 pounds are known(EC50,48h for their112.3 nematicidalg mL or) as nematostatic sterol, thiophene, activity flavonoid, against other and alkaloid-likenematode compounds (Figure1). Some of these compounds are known for their nematicidal or nematostatic species. activity against other nematode species. Figure 1. Structure of compounds identified from nematicidal extracts against J2 individuals of N. aberrans (1–11) and Figure 1. Structure of compounds identified from nematicidal extracts against J2 individuals of N. α-ecdysoneaberrans structure. (1–11) and α-ecdysone structure. 2. Results and Discussion Molecules 2021, 26, 2216 3 of 13 2. Results and Discussion 2.1. Nematostatic
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