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Sarri, K.; Mourouzidou, S.; Ntalli, N.; Monokrousos, N. Nematicidal Activity of Essential Oils and Root-Knot Nematodes. Encyclopedia. Available online: https://encyclopedia.pub/entry/54461 (accessed on 14 June 2024).
Sarri K, Mourouzidou S, Ntalli N, Monokrousos N. Nematicidal Activity of Essential Oils and Root-Knot Nematodes. Encyclopedia. Available at: https://encyclopedia.pub/entry/54461. Accessed June 14, 2024.
Sarri, Konstantia, Snezhana Mourouzidou, Nikoletta Ntalli, Nikolaos Monokrousos. "Nematicidal Activity of Essential Oils and Root-Knot Nematodes" Encyclopedia, https://encyclopedia.pub/entry/54461 (accessed June 14, 2024).
Sarri, K., Mourouzidou, S., Ntalli, N., & Monokrousos, N. (2024, January 29). Nematicidal Activity of Essential Oils and Root-Knot Nematodes. In Encyclopedia. https://encyclopedia.pub/entry/54461
Sarri, Konstantia, et al. "Nematicidal Activity of Essential Oils and Root-Knot Nematodes." Encyclopedia. Web. 29 January, 2024.
Nematicidal Activity of Essential Oils and Root-Knot Nematodes
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The Meloidogyne genus is widely recognized for its significant economic and scientific importance within the group of plant-parasitic nematodes. The chemical management of nematodes presents its challenges and heavily depends on employing soil fumigants containing toxic and costly nematicides. However, plant-derived essential oils offer promising alternatives, demonstrating a wide range of biological activities that affect nematodes through a range of mechanisms, including disrupting their nervous systems, inducing detrimental effects on plasma membrane permeability, penetrating the gelatinous matrix of nematode eggs, and disturbing intracellular redox status. Most of the extracted essential oils were predominantly sourced from the Lamiaceae family (32%), followed by Asteraceae (11%), Apiaceae (9%), and Poaceae (8%), and with genera Thymus, Mentha, Ocimum, Artemisia, Cymbopogon being the most common. The nematicidal activity of EOs primarily arises from their chemical groups, such as terpenes, phenylpropanoids, and organosulfur compounds. 

Meloidogyne bionematicides green nematicides nematode management

1. Introduction

Plant-parasitic nematodes (PPNs) pose a significant challenge to crop production, with root-knot nematodes (RKNs) being particularly threatening to global food security [1]. The Meloidogyne genus is widely recognized for its significant economic and scientific importance within the group of plant-parasitic nematodes. These nematodes exhibit high plasticity and adaptability, thriving in diverse geographical areas such as tropical and subtropical regions, like Africa, Asia, North and South America, and Europe [2]. According to indications from the Intergovernmental Panel for Climate Change, elevated temperature and moisture levels may result in an increased rate of infection, development, and reproduction, which, in turn, leads to the shift of their abundance and geographic distribution [3]. The Meloidogyne infect monocotyledonous and dicotyledonous plant species, inducing transcriptional reprogramming in host cells, leading to the formation of giant cells, establishing a permanent feeding site within the plant host where they obtain nutrients while completing their parasitic lifecycles [1][2][3][4]. These nematodes are sedentary endoparasites with four prevalent species (M. arenaria, M. hapla, M. incognita, and M. javanica). Recent research has revealed the existence of new species previously mistaken for one of the common four. Although the overall documented species count approaches 100, some of these species have more limited or poorly characterized host ranges [5]. Furthermore, Meloidogyne spp. can form dynamic disease complexes (MDCs) in conjunction with fungal and bacterial species, further exacerbating disease occurrences and, therefore, causing extensive damage to numerous vital crops globally, including tomato and coffee [6].

2. Essential Oils, Chemical Groups of Their Components, and Their Mode of Action

Over the last decade, there has been a particular interest in the nematicidal activity of plant EOs and their constituents [7]. The plant-derived substances have shown potential as a source of highly effective pesticidal compounds. They are regarded as an almost boundless reservoir of eco-friendly pest management solutions, with minimal impact on plant and human health, being easily biodegradable [8]. Essential oils comprise complex blends of volatile organic compounds naturally synthesized within various plant parts, forming part of the plant’s secondary metabolism. These metabolites, produced in response to various forms of biotic stress, play essential physiological roles, e.g., attracting pollinators, establishing symbiotic relationships, and providing structural components for lignified cell walls in vascular tissues. Additionally, they enhance ecological competitiveness, exerting diverse effects on the host plant and surrounding organisms [9]. A wide range of PSMs includes flavonoids, phenolic compounds, terpenes, and nitrogen-containing chemicals derived from primary compounds [10][11]. Although some PSMs are naturally produced and stored during regular plant growth, others are specifically synthesized in response to various stress conditions [8]. Essential oils are extracted from various plant parts like leaves, flowers, seeds, and bark. Extraction methods vary depending on the plant part used; steam distillation is the most common method due to its simplicity and cost-effectiveness. Other techniques include mechanical extraction, hydrodistillation, solvent extraction, supercritical CO2 extraction, and subcritical water extraction [12][13][14]. The chemical composition, toxicity, and bioactivity of the extracts, in turn, can be influenced by several factors, such as the phenological age of the plant, the percent humidity of the harvested material, and the method of extraction [15].
The nematicidal activity of EOs primarily stems from their individual components, such as specific chemical compounds or bioactive molecules (Figure 1). In various experiments, most of the components tested as nematicides are terpenes. Terpenes are formed structurally by coupling different numbers of isoprene units (5-carbon-base; C5), and they may or may not contain oxygen (terpenoids and terpenes). The main terpene classes are monoterpenes (C10), sesquiterpenes (C15), hemiterpenes (C5), diterpenes (C20), triterpenes (C30), and tetraterpenes (C40). The lipophilic nature of essential oils, including their terpenoid components, has been associated with in vitro cytotoxic activity, primarily due to the presence of phenols, aldehydes, and alcohols [16]. Terpenes exhibit nematode-targeting mechanisms by disrupting plasma membrane permeability due to their lipophilic properties. This disruption compromises barrier function and leads to the leakage of cytoplasmic macromolecules in various organisms, including plant-parasitic nematodes [17]. An alternative hypothesis regarding their impact on plant nematodes suggests a biochemical interaction mechanism where plants release compounds that exhibit toxicity towards both microorganisms and nematodes. The mode of action of each terpene is different and is inextricably linked to its chemical structure. Certain monoterpenes have been found to disrupt the structure of biomolecules like polysaccharides, fatty acids, and phospholipids and can induce depolarization of mitochondrial membranes [18][19]. Furthermore, Kalaiselvi et al. [20] mentioned another mode of action where monoterpenes of the essential oil of Artemisia nilagirica disturb the intracellular redox status, activate the central signaling pathway of apoptosis, and induce DNA damage, ultimately leading to cell death. Additionally, other components of EOs with nematicidal effects, not belonging to the terpene group, include organosulfur compounds such as allyl isothiocyanate (AITC), diallyl disulfide (DADS), and diallyl trisulfide (DATS). These compounds influence nematodes’ neurotransmission and chemosensing functions [21]. Phenylpropanoids, another group of components found in plant essential oils, show promising results against nematodes, including (e)-cinnamaldehyde, benzaldehyde, eugenol, and eugenol methyl ester. The well-characterized biosynthetic pathway of phenylpropanoids presents a promising target for enhancing nematode resistance, as enzymes involved in this pathway are induced in plants upon wounding or pathogen infection, including sedentary endoparasitic nematodes [22]. In more precise terms, oils containing phenylpropanoid aldehydes exert their effects against nematodes by impeding the activity of the V-ATPase enzyme. This enzyme, known as a vacuolar-type proton-translocating ATPase, is responsible for pumping protons across membranes and is energized by ATP hydrolysis. It plays critical roles in nematode nutrition, osmoregulation, cuticle synthesis, neurobiology, and reproduction [23]. Moreover, the presence of phenols, aldehydes, and alcohols in an EO can act against the nematode by disrupting the integrity of its cytoplasmic membranes [23].
Figure 1. Compounds of EOs and their mode of action against root-knot nematodes.
Many of the extracted essential oils renowned for their diverse biological properties predominantly originate from the Lamiaceae family (Table 1). The Lamiaceae family encompasses 7530 species, including trees, shrubs, subshrubs, and herbs. It is globally distributed and utilized across various fields, such as medicine, pharmaceuticals, and the food industry [24][25]. Within this family, EOs derived from genera like Thymus (e.g., Thymus vulgaris), Origanum (e.g., Origanum vulgare), Salvia (e.g., Salvia rosmarinus), Mentha (e.g., Mentha spicata), and Ocimum (e.g., Ocimum basilicum), have exhibited strong insecticidal, acaricidal, fungicidal, herbicidal and nematicidal properties [25][26]. Mint (Mentha spp.) stands as one of the most extensively studied plants for EO extraction, followed by thyme (Thymus spp.) and basil (Ocimum spp.). Additionally, significant amounts of EOs were derived from Asteraceae, Apiaceae, and Poaceae botanical families, with genera like Artemisia and Cymbopogon being prominent EO sources (Table 2).
Table 1. Plant sources of the essential oils belonging to the family Lamiaceae, their components with nematicidal action in different experimental settings against Meloidogyne spp.
Table 2. Plant sources of the essential oils belonging to different botanical families, their components with nematicidal action in different experimental settings against Meloidogyne spp.
The nematicidal effect of specific substances is closely linked to their chemical profile. The results indicate that compounds featuring hydroxyl (-OH) or methoxy (OCH3) groups, such as linalool, geraniol, carvacrol, and thymol, exhibited a higher frequency of nematicidal action compared to those with an acetyl group (acetyleugenol). This finding implies that the positions of the double bond within the propenyl group and the position of the substituent in the geometrical isomer play crucial roles in determining the nematicidal activity. Furthermore, allylic alcohol and phenolic alcohols, such as carvacrol and geraniol, demonstrated more potent nematicidal properties compared to other alcoholic compounds containing a hydroxyl group [39]. To differentiate the impact of essential oils based on their specific chemical compositions, researchers conduct identification and quantification of the constituent compounds of essential oils that are responsible for nematoxicity. This analysis involves techniques such as gas chromatography–mass spectrometry (GC–MS), high-performance liquid chromatography (HPLC), and proton nuclear magnetic resonance (HNMR) alongside in vitro assays [39][55].

3. Synergistic and Antagonistic Interactions among Essential Oil Components

Numerous compounds found in essential oils exhibit diverse mechanisms of action. The same chemical constituent may demonstrate distinct biological activity when included within a natural mixture compared to its isolated form. Therefore, natural compounds, when combined, can either enhance, complement, or attenuate each other [56]. Consequently, the utilization of these compounds together may result in various outcomes: zero interaction, synergy (where the response is greater than expected), or antagonism (where it is less) (Figure 2) [57][58]. Understanding the interaction between molecules is particularly crucial in agriculture, where effective bioactive substances are sought [59]. More specifically, recognizing the synergism of binary mixtures is essential for formulating artificial blends and developing new nematicides. The primary compounds found in the essential oils of M. didyma and M. fistulosa, namely carvacrol, γ-terpinene, and o-cymene, were investigated for their binary combinations, revealing reduced efficacy against Meloidogyne species. Notably, the combination of o-cymene and carvacrol at a 1:2 ratio resulted in the highest mortality rate at 31.5%, while the combination of γ-terpinene and carvacrol at a 1:2 ratio resulted in a mortality rate of 36.1%. Conversely, the combination of γ-terpinene and o-cymene at a 2:1 ratio exhibited the lowest mortality rate at 20.3%. This indicates the presence of antagonistic interactions among these compounds. Furthermore, both major and minor compounds within the EOs of M. didyma and M. fistulosa showed complex synergistic and antagonistic effects, as demonstrated by their heightened toxicity against M. incognita (LC50 at 1 μg/mL for 24 h) compared to individual tests [29].
Figure 2. Synergistic and antagonistic interactions between the components of essential oils. Reported synergies were extracted from studies by [29][35][38][51][60].
An additional interaction involving carvacrol is noted by Pardavella et al. [44], where the EO of Satureja Hellenica proved more effective against M. incognita than the corresponding hydrolat. One of the differences between the compounds of these two was the presence of p-cymene in the EO, which is crucial for nematicidal activity. This occurs due to its synergistic interaction with carvacrol; however, in this case, other substances, even in smaller quantities, might contribute synergistically. Furthermore, synergistic interactions were observed between carvacrol and geraniol, as well as between carvacrol and trans-anethole, showcasing the effectiveness of Thymus citriodorus EO and hydrosol against nematode paralysis [57].
Eloh et al. [35] conducted a study investigating compounds from the EOs of three plant species—Ocimum sanctum, Cymbopogon schoenanthus Speng, and Cinnamomum zeylanicum Blume. These compounds, primarily categorized as phenylpropanoids, displayed notable nematotoxicity, all exhibiting effectiveness (all showing EC50/48 h < 300 mg/L). The authors explored the synergistic potential of these compounds when combined with benzyl benzoate and carvone, a compound often associated with synergistic activities alongside EO components. Conversely, pairs that acted antagonistic were eugenol /isoeugenol, acetyl eugenol/ benzyl benzoate, cinnamyl alcohol/ eugenol, cinnamyl acetate/ acetyleugenol, cinnamyl alcohol/ isoeugenol, and acetyl eugenol/ isoeugenol. The components that showed additive effects were benzyl benzoate /eugenol, cinnamyl acetate/ eugenol, benzyl benzoate/ cinnamyl acetate, isoeugenol/ carvone, and cinnamyl alcohol/ carvone. Carvone showed synergistic activity with benzyl benzoate, methyl eugenol, and cinnamyl acetate. The synergistic nematicidal activity of carvone and phenylpropanoids may be explained by the differing modes of action between phenylpropanoids and terpenes. Although carvone effectively inhibits acetylcholinesterase, phenylpropanoids induce oxidative stress. The combination of these mechanisms has the potential to significantly enhance the nematicidal activity of the formulations [35].
Further synergy was documented in a study by Jardim et al. [60], where garlic EO displayed remarkable efficacy against J2 mortality and immobility, hatching inhibition, and reduction of eggs and galls in soil. The two main components of the oil, diallyl trisulfide (DATS) and diallyl disulfide (DADS), were found to exhibit a synergistic effect. The combination of DADS and DATS immobilized and killed a larger number of J2s compared to the sum of their individual effects. Interestingly, when DADS and DATS were tested individually, they could not match the immobility or mortality values of the essential oil at proportional concentrations. However, when combined, their activity surpassed that of the essential oil. For instance, a 56 μg mL−1 solution of DATS + DADS (14 + 42 μg mL−1, respectively) immobilized and killed 100% of J2s, while the essential oil at 62 μg mL−1 achieved 85.5% immobility and 82.3% mortality of J2s. These findings imply that other components of the EO interfere with the action of DADS and DATS against M. incognita J2.
A similar scenario was observed in the case of Cymbopogon schoenanthus, where the EO exhibited toxicity to M. incognita J2 with an EC50/72 h value of 288 mg/L after 24 h. However, its main compound, piperitone, failed to demonstrate any nematicidal activity at 500 mg/L. Hence, the nematotoxicity of the EO may be attributed to other single major components or synergistic interactions with piperitone [35]. The two major components of EO derived from black pine—α-pinene and c-verbenol—did not affect M. javanica, but the concentration of 1 μg/mL showed J2 mortality 81, 48%, indicating that synergies among the other minor components caused the nematicidal action [51].

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