Abstract
Root-knot nematodes (Meloidogyne spp.) are sedentary endoparasites and soil-borne pathogens worldwide. M. incognita is one of the most devastating and dominant species among them causing economic yield losses in almost all vegetables and other agricultural crops in the world. Current management strategies against M. incognita are not sufficient. However, from the last decades, utilization of nematicides has been increasing to manage this pest due to which environmental and human health issues arises. Bio-organic approaches are the best alternatives to nematicides, including biological agents and organic matters. In bio agents both arbuscular mycorrhizal and nematophagous fungi have a potent ability to manage plant-parasitic nematodes by inducing systemic resistance and activation of pathogenesis related (PR) genes in inoculated plants against nematodes, whereas nematophagous fungi trap nematodes for their feeding and killing them. Soil application of organic matters viz., botanical extract, oil cakes and agricultural wastes both in vitro and in vivo is also useful. Botanical extracts, oil cakes, kill nematodes by releasing secondary metabolites and inhibiting the movement of juveniles in the soil. Researchers from all over the world engage in evolving eco-friendly approaches that enhance and sustain the vegetable and agricultural production against this pest and keep it below the threshold level without affecting beneficial soil microbiota. In the future, such environment benign approaches have become an active field of research that adds new knowledge for their success against pest management, and enhancement of agricultural production for the human population.
Zusammenfassung
Wurzelgallennematoden (Meloidogyne spp.) sind sesshafte Endoparasiten und bodenbürtige Krankheitserreger weltweit. M. incognita ist eine der verheerendsten und dominantesten Arten unter ihnen und verursacht wirtschaftliche Ertragseinbußen bei fast allen Gemüsearten und anderen landwirtschaftlichen Kulturen in der Welt. Die derzeitigen Strategien zur Bekämpfung von M. incognita sind nicht ausreichend. In den letzten Jahrzehnten wurden jedoch immer mehr Nematizide zur Bekämpfung dieses Schädlings eingesetzt, was zu Problemen für die Umwelt und die menschliche Gesundheit führte. Bio-organische Ansätze sind die beste Alternative zu Nematiziden, einschließlich biologischer Wirkstoffe und organischer Stoffe. Bei den biologischen Wirkstoffen haben sowohl arbuskuläre Mykorrhizapilze als auch nematophage Pilze die Fähigkeit, pflanzenparasitäre Nematoden zu bekämpfen, indem sie eine systemische Resistenz und die Aktivierung von PR-Genen (pathogenesis related) in den beimpften Pflanzen gegen Nematoden induzieren, während nematophage Pilze die Nematoden einfangen, um sie zu fressen und zu töten. Der Einsatz von organischen Stoffen im Boden, d. h. Pflanzenextrakten, Ölkuchen und landwirtschaftlichen Abfällen, ist sowohl in vitro als auch in vivo nützlich. Pflanzenextrakte und Ölkuchen töten Nematoden ab, indem sie sekundäre Metaboliten freisetzen und die Bewegung von Jungtieren im Boden hemmen. Forscher aus der ganzen Welt arbeiten an der Entwicklung umweltfreundlicher Ansätze, die die Gemüse- und Agrarproduktion gegen diesen Schädling verbessern und aufrechterhalten, ohne die nützliche Bodenmikrobiota zu beeinträchtigen. In der Zukunft werden solche umweltfreundlichen Ansätze ein aktives Forschungsgebiet sein, das neue Erkenntnisse über den Erfolg bei der Schädlingsbekämpfung und der Verbesserung der landwirtschaftlichen Produktion für die menschliche Bevölkerung liefert.
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Introduction
The rhizosphere has numerous soil-borne microorganisms interacting with plant roots either antagonistically or synergistically and with other associated microbes. Few of them are helpful to plants and the rhizosphere, whereas some are harmful, i.e., act as biotic stressors. Plant-parasitic nematodes (PPNs) are the most critical and common soil-borne pathogens that affect the global agricultural industry (Kenney and Eleftherianos 2016). At present, about 4100 species of PPNs have been identified, which exhibit a negative impact on the agricultural industry by deteriorating numerous vegetable crops, including eggplant, okra, tomato, chilli, carrot, spinach, cabbage, cauliflower, etc. (Decraemer and Hunt 2013; Chariou and Steinmetz 2017). Numerous nematologists categorized top 10 PPNs that have a global economic impact; these are root-knot nematodes (Meloidogyne spp.), root lesion nematode (Pratylenchus spp.), cyst nematodes (Heterodera and Globodera), burrowing nematode (Radopholus similis), pine wilt nematode (Bursaphelenchus xylophilus), stem and bulb nematode (Ditylenchus dipsaci), reniform nematode (Rotylenchulus reniformis), rice white tip nematode (Aphelenchoides besseyi), false root-knot nematode (Nacobbus aberrans) and dagger nematode (Xiphinema index-the virus vector nematode) (Jones et al. 2013). Among these, root-knot nematodes (Meloidogyne spp.) are the most dangerous and economically important.
Meloidogyne incognita and Its Status On Vegetable Crops
Root-knot nematodes (Meloidogyne spp.) belonging to the family, Heteroderidae Order, Tylenchida are considered as highly adaptive, widespread and sedentary obligate endoparasites among all PPNs that completely depend on the host for their survival and reproduction (Khan 2008). Globally, > 100 species of root-knot nematodes (Meloidogyne spp.) have been identified with more than 3000 host plants, including vegetables and fruits. Four species viz., M. incognita, M. javanica, M. arenaria and M. hapla are major and more pathogenic to cause major losses to agricultural crops worldwide up to 90% and predispose the crops to other soil-borne pathogens (Hunt and Handoo 2009; Lunt et al. 2014).
According to Ghule et al. (2014), 14 species of root-knot nematodes have been identified from different areas of India. Out of different species of root-knot nematodes, M. incognita was the dominant species in agricultural fields that causes major loss and reduces the quality of vegetable crops viz., okra, eggplant, tomato, and spinach. However, the occurrence of root-knot disease in vegetable fields in different areas of India was predominant due to which vegetable qualities and production are affected. Other species viz., M. javanica, M. arenaria and M. graminicola are also common and pathogenic (Ghule et al. 2014). However, M. hapla is found in temperate/cooler areas (Escobar et al. 2015).
Annual vegetable losses reach up to 19.6%, whereas annual crop damage is up to the tune of Rs. 242.1 billion due to PPNs in India (Ahmad et al. 2021). Globally, an average of 10% annual yield loss is recorded in vegetables due to root-knot nematodes. However, much higher percentage losses have been recorded depending upon nematode species, and their population in the soil, locality, and crop species (Collange et al. 2011). Jain et al. (2007) reported yield losses up to 18.20%, 16.67%, 14.10%, 21.35%, 10.54%, and 27.21% in cucurbits, brinjal, okra, jute, rice, and tomato, respectively in India due to root-knot nematode, M. incognita (Table 1).
Life Cycle of M. incognita On Vegetable Crops
The life cycle of M. incognita i.e., from egg to mature female is completed in 25 days at 27 °C, but this period is altered by the availability of suitable host, soil moisture (lesser extent), and soil temperature (widely) (Fig. 1). It started with the hatching of second-stage juveniles (J2s), named to be an infective stage; a stage that initiates the process of infection into the host roots (Rawal 2020). However, CO2 is a major root diffusate that plays a significant role in long-distance attractant for J2s of M. incognita and other PPNs (Robinson 2002). After attaching with the host roots, J2s secret certain proteins or enzymes viz., endoxylanases, cellulases (endoglucanases), polygalacturonases and pectatelyases from their sub ventral glands into the roots (Davis et al. 2011; Wieczorek et al. 2014; Perry and Moens 2011). Some of these secreted enzymes change the components of the host plant’s cell wall or inhibit the host cell cycle, increase degradation of host cell protein, and reduce defence and transcriptional regulation (Akker and Birch 2016). Some parasitic enzymes digest the cellular component of the host plant, establish the permanent feeding site of nematodes within the host roots and help in the formation of giant cells (GCs) (Shakeel et al. 2020). GCs become galls or knots by hypertrophy and hyperplasia and are source of mineral nutrients for nematodes till reproduction. The formation of galls in the roots (Fig. 2) damage the vascular system of the host plant and inhibits its ability to absorb essential mineral elements and water from the soil that ultimately leading to wilting and yellowing of plant (Gao et al. 2016; Lee and Kim, 2016; Jamal et al. 2017). Such infections on the plants also increase the plant’s susceptibility to other soil-borne pathogens and form disease-complexes with other harmful soil microbes (Zhou et al. 2016).
Bio-organics Management
Continuous use of nematicides increases the environmental pollution and human health issues. Such issues enhance the utilisation of eco-friendly like bio-organic approaches that could be a grateful for managing M. incognita and sustain vegetables production. Although, cultural methods are traditional and facing more restrictions due to the wide host range of M. incognita and the existence of mixed populations of different species of genus, Meloidogyne in the field (Xiang et al. 2018), uses of resistant cultivars have been also a successful management tool to protect the crop, but it has been found that certain new species of root-knot nematodes break this resistance viz., M. enterolobii (Xiang et al. 2018; Hajihassani et al. 2019). Bio-organics management as eco-friendly management included biotic, application of microbes in both in vitro and in vivo conditions and abiotic/organic approaches, uses of botanicals, oil cakes and agricultural wastes. Besides these, plants themselves also manage several types of soil-borne pathogens, including M. incognita, by releasing various root exudates, namely amino acids, sugars, organic acids etc. (Bell et al. 2019).
Biotic Approaches Against M. incognita
In biotic approaches, application of living agents’ viz., fungi (arbuscular and nematophagous fungi), bacteria or other microbes are considered. These bio agents consists of factors or substances that improve plant growth by inducing resistance gene and control PPNs is another best tool which replaces the chemicals in agriculture (Forghani and Hajihassani 2020). Several studies suggested that synthetic pesticides or chemicals create environmental issues. The excessive amount of chemicals in the soil reduces its fertility, builds soil disintegration, and has negative impacts on human health. Bio-agents will help the plants to control or reduce the harmful effects of soil-borne pathogens, including root-knot nematode, M. incognita by interacting with the roots of plants (Forghani and Hajihassani 2020). Other activities like facilitating the resources acquisition, production of plant hormones (gibberellins and cytokinin), lytic enzymes and antibiotics also are done by beneficial microbes within the soil (Glick 2012). Some of the mechanisms were involved to facilitate the endogenous defence at the gene level by activating the genes related to pathogenesis (PR-genes), PR‑1, PR-1b, PR‑3, 5, salicylic acid (SA)-dependent genes related to pathogenesis of the systemic acquired resistance (SAR) and other genes that kill M. incognita. Few enzymatic activities like endochitinase and glucanases were also increased against M. incognita in the roots of pre-treated inoculated plants (Molinari and Leonetti 2019).
Arbuscular Mycorrhizal Fungi (AM Fungi) as Bio-control Agents Against M. incognita
Arbuscular mycorrhizal fungi (AM fungi) are found in greater than 80% of almost all soil plants species as obligate root symbionts. They increase uptake of mineral elements in their host plant in exchange of carbon, enhance plant growth and reduce stress in plants (biotic and abiotic stress) (Smith et al. 2010; Vos et al. 2012). These fungi also help plants to increase water uptake and reduce metal toxicity in the soil (Kerry and Hominick 2002). Several studies, in vitro and in vivo revealed the protective effects of AM fungi against root-knot nematodes in some plants viz., in tomato against M. incognita, in coffee against M. exigua, M. cofeeicola and in banana against X. index (Vos et al. 2012; Koffi et al. 2013). AM fungi also facilitated the plants to produce certain compounds against PPNs and interfered in the secretion and production of root diffusates that attract PPNs (Teillet et al. 2013).
Mechanisms of Action of AM Fungi Against M. incognita
Enhanced Plant Tolerance
Increased Nutrients Uptake
AM fungi in their host plant facilitate the uptake of certain macro elements such as phosphorus, nitrogen, some micro element viz., zinc and water from the soil; in return, they take carbon from their host (Smith and Smith 2011; Baum et al. 2015). However, it has been found the plant that colonized by AM fungi showed higher phosphate uptake and less susceptibility to M. incognita in contrast to the plant that was not colonized by AM fungi. According to Pettigrew et al. (2005), higher nutrient uptake in cotton plant fields helped to reduce or control sedentary semi-endoparasitic nematode, Rotylenchulus reniformis.
Changed Root Morphology
In addition, to increase nutrients uptake, AM fungi inoculated plants showed higher root branching, growth, and led to change in root morphology like tap root than fibrous root from which plant improve their nutrient acquisition and better biomass (Gutjahr and Paszkowski 2013; Yang et al. 2014). According to Vos et al. (2014), mycorrhizal treated plant shows better root growth and branching, leading to resistant against M. incognita. AM fungus Funneliformis mosseae protect the banana plant from migratory endoparasitic nematodes Pratylenchus coffeae and Radopholus similis by increasing or changing root morphology (Elsen et al. 2003b). However, it has been reported by some researchers that increased in root branching lead to an increase in infection sites that negatively affect host plant. Depending on the plant species and PPNs viz., root-knot nematode, M. incognita and cyst nematodes (Heterodera spp.), prefer lateral root formation sites and elongation zones, whereas R. similis, prefers primary roots due to presence of secretory substances in these zones (Curtis et al. 2009; Elsen et al. 2003a).
Challenges for Nutrients, Space and Infection Sites
Competition for space, host nutrients and infection sites is found among microbes which occupy the same habitat and have the same feeding requirements in an ecological niche when resources are limited such as carbon (C) (Vos et al. 2014). Competition for nutrients like carbon becomes the main mechanism for AM fungi-mediated bio-control (Jung et al. 2012). AM fungi treated plants do better photosynthesis in which carbon demand increase such higher carbon demand inhibits pathogen growth.
Competition for the available space suggested that high level of AM fungi colonization within the host roots resulted in a higher level of bio-control activity against M. incognita (Vierheilig et al. 2008). However, a bio-control activity was observed when both AM fungi and M. exigua were inoculated in the coffee plants (Alban et al. 2013). Vigo et al. (2000) found that the AM fungi treated roots reduced the number of infection sites, revealing that more infections will be by pathogen infections.
Effect of Induced Systemic Resistance
It has been found that inoculation of tomato plants with AM fungi increased the systemic resistance against M. incognita (De la Peña et al. 2006). Plants have a specialized pattern called microbe-associated molecular patterns (MAMPs) between harmful and beneficial fungi (Zamioudis and Pieterse 2012). Recognition receptors on MAMPs help to switch on the MAMPs triggered immunity (MTI) which initiate the defence in plant against further invasion by PPNs (Jones and Dangl 2006). Activation of MTI responses leads to hormonal and transcriptional changes in their host plant (Schouteden et al. 2015). Fiorilli et al. (2011) evaluated the changes in the transcriptome of tomato plants when colonized by AM fungi F. mosseae. They reported significant modification in genes both in shoots and roots, with the highest variations in both primary and secondary metabolism and defence response against biotic stimulus such as root-knot nematode, M. incognita. AM fungus F. mosseae was involved in the activation of the root-specific 9‑lipoxygenase (9-LOX) and isoleucine conjugation of the jasmonic acid (JA-Ile) pathway. Activation of early MTI-response leads to the induction of jasmonate-linked 9‑LOX-pathway that inhibit the development and growth of root-knot nematode. Expression of the 9‑LOX gene (ZmLox3 gene) in maize plants was beneficial and enhanced protection against M. incognita (Gao et al. 2008). It has been observed that external JA-application and study of changes or mutants in the JA-pathway were found to initiate the resistance in host plant against PPNs (Fan et al. 2015; Fujimoto et al. 2011). Li et al. (2006) observed that the class III chitinase gene of Glomus versiforme in the roots of grapevine was activated during the infection by M. incognita. Such report strongly recommends that AM fungi’s class III chitinases gene provides resistance against the PPNs. Though the eggs with chitin are affected more by the chitinase enzymes, they also reduce the egg masses and number of the females of root-knot nematodes (Chan et al. 2015). However, future research should be focused on demonstrating the mechanism of action of chitinases against PPNs, with attention on the metabolome and proteome AM fungi-associated changes.
Altered Rhizospheric Interactions
Alteration in the release of root exudates affects the microbial community in the vicinity of roots and affects interactions between pathogen and plant (Lioussanne 2010). Some reports suggested that the colonization of a plant by AM fungi increased the diversity of beneficial microbes like Streptomyces species, fluorescent pseudomonads, chitinase-producing actinomycetes, and facultative anaerobic bacteria (Nuccio et al. 2013; Miransari 2011). These microbes showed antagonistic activity against root-knot nematodes and other PPNs, either by egg-parasitizing fungal activity or nematode-trapping activity or also by induction of the plant defence (Zamioudis and Pieterse 2012). Secretory substances from the roots of mycorrhizal plants were involved in the activation of the beneficial fungus Trichoderma spp. having bio-control activity against root-knot nematodes and attraction of plant growth-promoting bacteria Pseudomonas fluorescence (Druzhinina et al. 2011; Sikora et al. 2008) (Fig. 3).
Nematophagous Fungi as Bio-control Agents Against M. incognita
“Nematophagous fungi” are referred to a various group of fungi that feed and colonize on the nematodes. Some fungi parasitize nematodes are obligatory, whereas most of them are as facultative saprophytes of nematodes (Lopez-Llorca et al. 2008). These fungi belong to various phylogenetic groups, Zygomycota, Chytridiomycota, Ascomycota and Basidiomycota. The fungi of zygomycetes group are entirely dependent on water and encircle soil particles in searching of nematode hosts by their swimming zoospores. Based on the mechanisms of action against nematodes, nematophagous fungi can be classified into four major groups: (I) nematode-trapping fungi (predatory fungi), (II) endoparasitic fungi, (III) egg-parasitic fungi and (IV) toxin-producing fungi (Fig. 4; Table 2).
Predatory/nematode Trapping Fungi
Fungi of this group are soil-borne that trap moving stages of M. incognita with the help of various trapping structures of different size and shapes as shown in Table 2. The predatory nature of these fungi exists in the presence of nematodes prey and produces various types of trapping devices such as adhesive network, knobs, and columns, non-constricting and constricting rings through which they capture nematodes (Zhang and Hyde 2014). It was found that trapping fungi also have the capability to release certain compounds as antimicrobial and nematicidal properties, pleurotin (Nematoctonus robustus, N. concurrens) or linoleic acid (Arthrobotrys oligospora and A. conoides) viz., A. superba secret a compound for trapping J2s of M. incognita (Hallmann et al. 2009). However, soil applications of various substances like organic compounds (chopped leaves, oil cakes) and glucose increases the trapping ability of nematode-trapping fungi (Duddington 1962; Cooke 1962). Nematode trapping ability of Drechslerella stenobrocha strain AS6.1 was enhanced by soil application of abscisic acid (ABA) and inhibited by nitric oxide (NO) (Xu et al. 2011). It has been found that A. dactyloides efficiently trapped pathogenic juveniles of M. graminicola compared to Dactylella brochopaga and Monacrosporium eudermatum (Hallmann et al. 2009).
Endoparasitic Fungi
Endoparasitic fungi infect M. incognita using their spores (conidia or zoospores) and complete their vegetative phase inside nematode (Lopez-Llorca et al. 2008). However, as compared to trapping fungi, endoparasitic fungi consist of either a limited saprophytic phase or no saprophytic phase (Moosavi and Zare 2012). The conidia of endoparasitic fungi adhere to the nematode cuticle with the help of hyphae and kill them. Other endoparasitic fungi like Nematoctonus spp., Drechmeria coniospora and Haptocillium balanoides, are extensively studied and have a potent practical approach for controlling PPNs such as Meloidogyne spp. compared to nematode trapping fungi of which D. coniospora is the most studied against root-knot nematode (Viaene et al. 2006). However, in-vitro studies showed that Hirsutella rhossiliensis caused the death of M. incognita J2s in 2 days, whereas Ditylenchus dipsaci in 4 days (Cayrol et al. 1986).
Egg Parasitic Fungi
Fungi parasitizing eggs, female and other stages of PPNs, attracted more attention due to their potent approach in controlling economically important nematodes viz., root-knot nematode, M. incognita and cyst nematodes (Heterodera spp.). These fungi infect their host nematodes with the help of specialized structures called zoospores, appressoria, lateral mycelial branches and penetration peg (Lopez-Llorca et al. 2008). Paecilomyces lilacinus, Pochonia chlamydosporia and Lecanicillium psalliotae are the most frequently isolated and promising bio-control agents against M. incognita among all egg parasitic fungi (Li et al. 2015). The egg shell layer of M. incognita consists of chitin and protein organized in an amorphous and microfibrillar structure degraded by several hydrolytic enzymes like proteases and chitinases of egg parasitic fungi (Yang et al. 2007a).
Toxin Producing Fungi
The toxin-producing fungi are the most prominent and more potent against PPNs. These fungi release toxins that show nematicidal properties and paralyse the nematodes before penetration of fungal hyphae through nematode cuticle (Lopez-Llorca et al. 2008). Fungus, Pleurotus ostreatus released a potent toxin named trans-2-decenedioic acid, showing both in vivo and in vitro nematicidal properties and quickly paralysed the PPNs (Luo et al. 2004).
Besides the four groups of nematophagous fungi, some other fungal species of genus, Trichoderma is considered a good bio-control agent that produces a variety of enzymes against M. incognita, and secrets plant growth-promoting compounds (Agrawal and Kotasthane 2012). Trichoderma spp. secret extracellular hydrolytic enzymes viz., serine protease (SprT), trypsin like proteas (PRA1) and chitinolytic (chi18‑5 and chi18-12) that can parasitize nematode larva and eggs (Szabo et al. 2012). Comparative evaluation of protease enzyme expression in T. harzianum revealed that 13 peptidase encoding genes with the addition of aspartic protease genes P6281 and P9438, acidic serine protease gene PRA1, sedolisin protease gene P5216 and metalloendopeptidase gene P7455, all these genes play a major role in parasitising M. incognita eggs (Szabo et al. 2013). Trichoderma spp. were also involved in the release of some other nematicidal compounds like β‑vinylcyclopentane-1α, 3α-diol, 6‑pentyl-2H-pyran 2‑one, trichodermin, and 4‑(2-hydroxyethyl) phenol (Yang et al. 2012). However, the hatching of Meloidogyne spp. eggs were also inhibited by the cultural filtrates of Trichoderma isolates. This inhibition was directly proportional to the cultural filtrate concentration and the time of exposure (Rompalli et al. 2016).
Mechanisms of Action of Nematophagous Fungi Against M. incognita
The methods by which nematophagous fungi infects/kill root-knot nematode, M. incognita takes place by the process like attraction/recognition, adhesion, penetration and digestion through enzymatic action (Dong and Zhang 2006).
Attraction and Recognition of Nematodes
Attraction and recognition is the initial stage during the mechanism of nematodes infection by nematophagous fungi, during such process cell-cell communication and involvement of a range of interactions viz., physiological, biochemical or morphological taking place between fungi and M. incognita. The process of attraction and recognition were facilitated by certain volatile organic compounds (VOCs) secreted by the nematophagous fungi (Wang et al. 2010). Various VOCs include terpenoid (camphor), monoterpenes (α-pinene and β‑pinene) released from the pine tree during the infection by pinewood nematode, Bursaphelenchus xylophilus. However, it has been found that endoparasitic fungus, Esteya vermicola mimics the scent of such VOCs that released from the pine tree infected by pinewood nematode (Lin et al. 2013). Although it has been found that nematode, Neoaplectana glaseri released a putative morphogenic signal (nemin) that induces trap formation in A. conoides, a compound ascaroside was also involved to induce of trap formation and adhesive network against nematodes in A. oligospora (Hsueh et al. 2013). According to Li et al. (2007), G proteins are the major proteins that act as sensors, inducing the pathogenesis, response to environmental signals and constricting-ring formation in A. dactyloides.
Adhesion to Nematodes Shell or Cuticle Through Adhesive Proteins
Adhesive proteins in nematophagous fungi are the polymer of extracellular fibrils and present on the spores or outer surface of traps of fungi and play major role for those fungi that adhered to the cuticle or shell of the root-knot nematode (Tunlid et al. 1991).
Lectins are considered as adhesive proteins that isolated from adhesive traps of nematophagous fungi, it functions as recognition of root-knot nematodes due to the presence of different glycosyls, like D‑glucose, D‑mannose and N‑acetyl-D-galactosamine (GalNAc) (Nordbring-hertz and Mattiasson 1979). Balogh et al. (2003) noticed that deletion of a gene code for lectin protein (AOL_s00080g288) from A. oligospora did not affect its pathogenicity against PPNs. Two lectin genes (fucose-binding lectin gene and GalNAc-binding lectin gene) occurred in the nematophagous fungus, D. stenobrocha genome, enhancing the pathogenicity of fungus against PPNs (Liu et al. 2014). Few other genes that code for potent fungal adhesion protein are also occured in the nematophagous fungal genome along with lectins for example, 12, 17, and 26 CFEM containing proteins are found in A. oligospora, D. stenobrocha, and D. haptotyla, respectively (Meerupati et al. 2013). Similarly, the occurrence of 6, 6, and 28 GLEYA-containing proteins that function like lectins was also suggested by Meerupati et al. (2013). Quantitative Polymerase chain reaction analyses of 17 adhesion proteins in A. oligospora having five genes, AOL_s00076g567, AOL_s00043g50, AOL_s00007g5, AOL_s00210g231, and AOL_s00076g207 were changed or coded for trap formation mechanism in A. oligospora against M. incognita (Yang et al. 2011).
Enzymatic Action of Nematophagous Fungi Against M. incognita
Extracellular enzymes, such as collagenases, serine proteases, and chitinases, causes breaking of nematode eggshells and cuticles facilitating fungal penetration and colonization (Yang et al. 2013).
Collagen Degrading Enzyme (Collagenases)
Such enzymes cause the degradation of collagen protein of nematodes. According to Tosi et al. (2002), almost all species under Arthrobotrys release collagenase enzymes. Other enzymes like glycoside hydrolases (GHs) are also played an important role in degradation of hemicellulose, cellulose, xylans, lignocellulose and other cellular constituents of PPNs including root-knot nematode (Gibson 2012).
Cuticle Degrading Protease (Serine Proteases)
Serine proteases are the most studied extracellular enzymes released by nematophagous fungi. Approximately 20 serine proteases were identified from various nematophagous fungi in which P32 serine protease was first discovered from the fungus, Pochonia rubescens (Verticillium suchlasporia) (Yang et al. 2007b). The phylogenetic study suggested that serine protease belongs to two lineages, (I) neutral protease from nematode-trapping fungi, (II) alkaline proteases from nematode-parasitic fungi (Li et al. 2010). Both of the proteases differ in electrostatic surface potential distributions, the flexibility of substrate-binding sites and catalytic and nematicidal activities (Liang et al. 2011). Although pathogenicity of nematophagous fungus, A. oligospora against PPNs was improved by its genetic changes, i.e., by inserting an additional copy of cuticle-degrading protease (PII) into its genome (Ahman et al. 2002).
Chitin Degrading Enzymes (Chitinases)
Egg shells of PPNs have a structural component known as chitin (40% w/w). Enzyme chitinases found in egg parasitic fungi were used to penetrate the egg shell of nematodes. The first chitinase Chi43 enzyme was isolated from two nematode eating fungi, P. rubescens and P. chlamydosporia (Tikhonov et al. 2002). Although 16 important genes that code for GH18 chitinases analysed from nematophagous fungi, A. oligospora and D. stenobrocha genomes respectively, provide nematicidal activities (Liu et al. 2014) (Fig. 5; Table 3).
Abiotic Approaches Against M. incognita
Various abiotic approaches were considered against M. incognita and farmers evaluated them to utilise as organics in their fields. Fortunately, they have been involved in controlling or keeping the PPNs population below the threshold level. Several researchers have reported the various organic products of plant origin, viz., botanicals, oil cakes, agriculture and industrial wastes have potent nematicidal and plant growth promoting properties after amending to the soil. Addition of these compounds to the soil enhance the releases of various metabolites from the plant such as alkaloids, terpenes, diterpenes, sesquiterpenes, fatty acid, glucosinolates, phenols and polyacetylenes which provide a defence to plants against pathogens including M. incognita (Thoden et al. 2011).
Mechanisms of Action of Various Organics Against M. incognita
Botanical Extracts Against M. incognita
Plant extracts have nematicidal properties, and they reduce not only the population of nematodes, but also stimulate the growth of the plant (Olabiyi and Ayeni 2016). More than 100 species of plants have been utilized for their antinemic activities. Few of them showed promising results in killing root-knot nematodes viz., Euphorbia caducifolia, Azadirachta indica, Calotropis procera and Nerium oleander. They also exhibited inhibitory effects against J2s of root-knot nematodes (Laquale et al. 2015). According to Yuhui et al. (2018), crude root extract of Fumaria parviflora contains nematicidal compounds like alkaloids, sterol and alcohol. These compounds reduced root galls and killed J2s of M. incognita and alcoholic containing compounds from F. parviflora like 23α-Homostigmast-en-3β-ol, and Nonacosane-10-ol showed synergistic effects on J2s of M. incognita on tomato. Wen et al. (2019) tested in vitro aqueous extract of two plants Paenoia rockii and Camellia oleifera against M. incognita, extract of P. rockii at 5 mg/ml caused 100% mortality or inactivation of J2s of M. incognita. In vivo experiment by using aqueous extracts of chinaberry fruits (Melia azedarach), researchers got success in the management of M. incognita and M. javanica and improved soil biological activity (Ntalli et al. 2018). Aqueous extract of garlic contains compound allicin (diallyl thiosulfinate), tested in vitro against root-knot nematode, M. incognita. In vitro study of allicin showed inhibitory effect against M. incognita. However, in vivo study of allicin showed that it enhanced tomato yield and reduced the population of M. incognita by increasing enzymatic activities like peroxidase, catalase and superoxide dismutase in tomato leaves compared to untreated control (Ji et al. 2019). Thus, allicin may be a potent alternative of chemical nematicides for the management of root-knot nematodes. Water extracts of fruits and leaves of Coccinia grandis and Ageratum conyzoides showed the mortality of J2s and inhibition of egg hatchability of M. incognita in vitro (Asif et al. 2017). According to Ntalli et al. (2020), lemon thyme powder (Thymus Citriodorus) enhanced the growth of tomato plants in a dose-response manner. When it was applied in the soil at 1 g kg−1, it exhibited nematicidal activity at a 95% level on M. incognita. D’Addabbo et al. (2020) tested in vitro aqueous extract of Medicago spp. (M. hybrid, M. murex, M. heyniana, M. lupulina, and M. truncatula) which have bioactive compounds, saponins that killed the J2s and inhibited egg hatching of M. incognita.
Plant Oil Cakes Against M. incognita
Oil cakes are an effective source of phosphorus, nitrogen and potassium (NPK) that improve the chemical, physical and biological activity of soil and inhibit the development of root-knot nematodes. Soil amended with different types of oil cakes which took about 10–14 days for decomposition after that releases nutrients for plant growth and eventually caused inhibition of the population of PPNs. Amendment of oil cakes in moist soil is more effective compared to dry soil. Amendment of mustard and neem cake into the soil was found to be effective against the multiplication of root-knot nematode. However, oil cakes from Jatropha sp. flax (Linum usitatisimum), mahua (Madhoca indica), sesame (Sesamum indicum), castor (Ricinum communis) and groundnut (Arachis hypogea) have been found effective in reducing the multiplication of root-knot nematodes (Rehman et al. 2015). Neem cake reduced the egg hatching, killing M. incognita J2s and also enhanced tomato growth and yield (Kumar and Khanna 2008). The application of neem cake effectively suppressed root-knot nematode, and increased the growth and yield parameters of cucumber (Devi and Das 2016).
Agriculture and Industrial Wastes Against M. incognita
Agricultural wastes can be characterised as plant parts or pieces that remain in the field after crop harvesting. These wastes may vary in their decomposition rate or properties like antinemic (Lal 2005). It improves soil’s chemical, physical and biological properties and manages root-knot nematodes after their proper and complete decomposition. Application of agricultural wastes like saw dust and rice husk into the soil inhibited the population of root-knot nematodes (Meloidogyne spp.) and enhanced growth and yield of tomato crop (Prakash and Singh 2014). Due to global industrialization and mass crop cultivation, it is important to invent a new method or process for changing industrial wastes into value-added products that could be utilized in controlling soil-borne pathogens like root-knot nematodes. Brito et al. (2020) were considering some agro-industrial waste viz., sugarcane bagasse, orange bagasse, poultry litter, and some other wastes to manage M. javanica in pots. Several wastes like soybean hulls, orange bagasse and others are most efficient in the control of root-knot nematodes up to 55–100%. Cassava (Manihot esculenta), starch industry releases a liquid residue known as Manipueira as good source of cyanogenic glycosides. It showed nematicidal effects against M. incognita by reducing galls or killing J2s and improved tomato yield (Nasu et al. 2015).
Essential Oils (EOs) Against M. incognita
Researchers and industrialist engage in the evaluation of essential oils (EOs) as bio-nematicides for the root-knot nematodes. EOs and other secondary metabolites extracted from plants were directly affected the root-knot nematodes, especially on the J2s and egg hatchability (El-Nagdi et al. 2017). In vitro testing of EOs from true myrtle (Myrtus communis) showed nematicidal activity against M. incognita (Ardakani et al. 2013). According to Onkendi et al. (2014), EOs from plants belonging to the family Asteraceae were utilized as management for root-knot nematodes. In vitro experiment showed that EOs were considered as soil bio fumigants for reducing galls or killing M. incognita J2s on tomato and enhancing its yield (Laquale et al. 2015). EOs from Mexican tea (Dysphania ambrosioides) have 99.08% of total oil with nematicidal activities, i.e., inhibited egg hatching by 100% and galls by 99.5%, further chromatography, mass spectrometry studies showed that oil from D. ambrosioides was composed of p-cymene (3.35%), (Z)-ascaridole (87.28%) and E‑ascaridole (8.45%). EOs from three Brazilian plants (Hyptis suaveolens, Astronium graveolens and Piptadenia viridiflora) were tested both in vitro and in vivo against M. incognita. Among them, Piptadenia viridiflora showed inhibitory effect against M. incognita due to the presence of major component, benzaldehyde. These component was able to inhibit egg hatching up to 65% and its oxime compounds were able to reduce galls up to 84% and egg hatching up to 89% on tomato plant (Barros et al. 2019b) (Fig. 6; Table 4).
Conclusion
When examining the significance of monetary damage due to root-knot nematode, M. incognita and the fact of the limitations by the government for the utilization of pesticides, it is important to researchers that there is a demand for the evolving new novel eco-friendly approaches against M. incognita. Several scientists are concerned about the excessive utilization of pesticides for controlling the crop pests by the farmers, and they pressurize the farmers to minimize the use of pesticides to overcome the environment pollution issues. This review mainly focused on the bio-organic management as eco-friendly for controlling of M. incognita. Biological agents and organic matters are the alternative for pesticides that do not only manage M. incognita as eco-friendly, but also improve growth and yield of vegetables. In biological agents, nematophagous fungi manage root-knot nematodes by cuticle penetration, absorption and digestion of nematode cuticle and AM fungi colonizes the rhizosphere, induced resistance in plants and compete with nematode and killing them. Organic soil amendments prompt the development of beneficial soil microbe’s population and reduce the population of nematodes or plant diseases as well as boost soil fertility, water holding capacity, physical properties of soil, and plant growth. Both soil amendments and the bio-control agents have been studied to some extent against root-knot nematodes. Still, with advancements in technology recently, there should be more profound studies on how these two approaches can synergistically affect nematodes and kill them. Whatever methods/strategies are invented, in future the focus is on the essential aspects like green approaches which manage root-knot nematodes without affecting environment and human health.
Abbreviations
- GalNac:
-
D-galactosamine N‑acetyl
- GCs:
-
Giant cells
- J2s:
-
Second stage juveniles
- MAMPs:
-
Microbe-associated molecular pattern
- MTI:
-
MAMPs triggered immunity
- PPNs:
-
Plant parasitic nematodes
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The authors are highly obliged to the Head of Department (Botany), Aligarh Muslim University, Aligarh, India for giving valuable suggestion regarding to the work.
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AK suggested the idea of the manuscript. AK, GA and MH find out the literature and wrote the complete manuscript. AAK has done the final editing of the manuscript. AK and MH compile and formatted the manuscript according to journal guidelines. AK is responsible for the correspondence of manuscript. The manuscript has been read and approved by all the authors.
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A. Khan, G. Ahmad, M. Haris and A.A. Khan declare that they have no competing interests.
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Khan, A., Ahmad, G., Haris, M. et al. Bio-organics Management: Novel Strategies to Manage Root-knot Nematode, Meloidogyne incognita Pest of Vegetable Crops. Gesunde Pflanzen 75, 193–209 (2023). https://doi.org/10.1007/s10343-022-00679-2
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DOI: https://doi.org/10.1007/s10343-022-00679-2
Keywords
- Meloidogyne incognita
- Arbuscular mycorrhizal
- Nematophagus fungi
- Induced systemic resistance
- Pathogenesis related genes
- Botanical extracts
- Oil cakes