1. Introduction

Plant-parasitic nematodes (PPNs) can cause significant losses in the size and quality of a wide range of economically important crops. Previously, regulatory and sanitation measures entirely avoided their casual introduction, minimized their spread, and/or reduced their damage. However, the current widespread and severe damage of PPNs lead to the need for additional control measures. Synthetic nematicides have shown some nematode control with consequent yield increase—but many of them have been restricted or banned. This is due to their adverse effects on human health and the environment, as well as damage to the durability of many agricultural ecosystems. Increasing concern over such chemical nematicides has led to unprecedented and great efforts in various research areas to manage these pests safely and effectively.

Current nematode research has addressed genetics and molecular patterns associated with plant defense and damage in the event of nematode infection ^[1]. Research has also addressed microbial priming ^[2], which has achieved tremendous progress. Various techniques are being developed to fully grasp the interaction between PPNs and their host and non-host plants via the elicitor-receptor reciprocal action ^[3][4]. These substantial mechanisms are expected to provide people with the needed information to design durable nematode resistance in plants. Moreover, the processes engaged in plant defense and protection against PPN can be activated by beneficial microbes and synthetic elicitors that can be soundly and effectively exploited ^[4].

Various aspects of the current research focus on the fundamentals of the PPN–plant relationship. However, there have been related opportunities to exploit the available applications to safely control nematodes. Thus, benign alternative methods to chemical nematicides are expected to make up many of the the durable crop protection strategies. Abd-Elgawad ^[5] recently addressed the general strategies of using safe antagonists of PPNs. They are generally based on either augmentation (inundative and inoculative) or conservation biological control. This review extends and updates implementations of such strategies. It highlights the use and potential of various strategies and tactics that can contribute to PPN management. Such approaches may include biological control agents (BCAs), the use of botanicals (e.g., antagonistic plants), host plant resistance to nematodes with related crop rotations, and other advanced treatments. The desired outcome is not only to avoid plant damage and yield losses caused by the nematodes and contribute as best people can in sustainable agricultural ecosystems, but to summarize current progress made in the research and application of these techniques. It also presents key factors affecting their success and broader exploitation, as well as their merits and demerits, and discusses agricultural practices that optimize PPN control.

2. Biological Control Agents

The obligate parasites, Pasteuria spp. , are extremely safe BCAs to manage PPNs. They can act on the nematodes under tough ecological conditions and with variable soil temperature, pH, and moisture. Their spores usually attach to the cuticle surface of the specific nematode species/race as they move about in the soil. Once adhered, they set up germ tubes that break into the nematode’s interior body. The internal proliferation of these cells and sporulation suppresses nematode multiplication and causes nematode mortality. As they are species-specific, Pasteuria spp. do not hurt non-target organisms, e.g., as a RKN-specific parasite, P. penetrans can only infect the related J 2. The attached spores restrict the nematode movement and make them stick to the nearby nematodes. If the PPN can mature, the female may produce a few or no eggs in host plants. Abd-Elgawad ^[5] reviewed the attributes which allow Pasteuria spp. to integrate with other safe approaches, e.g., crop rotation, soil amendments, and nematode-resistant cultivars, to manage PPNs. Their endospores are resistant to mechanical shearing, drying, and heat. However, Pasteuria isolates should be screened to select the most adequate one(s) for biocontrol in specific agroecosystems because they are very specific and may only attack certain isolates of a given species.

Suppressive soils were reviewed as those in which harmful pathogens and parasites, herein PPNs, cannot set up or persist, found, but lead to no disease, or become established and initiate a mild disease that soon recedes ^[6]. The biological activity of such a specific soil is documented when its suppressiveness: (1) is removed by biocides; (2) can be conveyed to conducive soil with a modest volume of suppressive soil; (3) is specific to a nematode species; (4) can reduce multiplication in root-knot and cyst nematodes in the root zone; (5) can be detected by baiting methods; (6) is heat sensitive; (7) is density-dependent. To achieve these attributes, the BCAs in nematode-suppressive soils can act directly as nematode antagonists and/or they can indirectly prime plants and induce their defense responses against PPNs. Antibiosis and parasitism by BCAs were also suggested in a few soils with specific PPN suppressiveness. Topalović et al. ^[7] appraised fungi and bacteria that were characterized in PPN-suppressive soils via next-generation sequencing or extracted from dead or diseased PPNs. They noted that soil suppression may act against the relevant PPN species as the microbiome may vary from one soil to another. For instance, suppressive soil was more efficient in M . hapla than the M. incognita control. Additionally, soil properties and plant species/cultivar can also influence the magnitude of this suppression. Thus, to avoid the impact of soil physicochemical and nutritional features, Topalovic et al. ^[8] altered the approach of transferring soil suppressiveness to the conducive soil by using the microbial component of the suppressive soil only in a water suspension. However, the soilless suspension could not cause mortality of any PPN species, but it could in tomato-planted soil with the suspension ^[8].

The magnitudes of root colonization by BCAs and their possible metabolites and induced resistance are impacted by plant genotype. Nematode-susceptible plants will harbor more PPNs and need more BCAs to suppress them than poor host plants. Although two isolates of P. chlamydosporia prompted systemic resistance against RKNs, the induction was plant species-dependent. This reduced M. incognita female fecundity, infection, and reproduction of tomatoes, but not cucumbers ^[6]. Moreover, in a separate monoculture of different sugar beet cultivars in Heterodera schachti -infested soil, H . schachtii -tolerant cv. “Pauletta” enabled suppressiveness to be set up without the initial yield decrease noted in susceptible cv. “Beretta” ^[9]. Botelho et al. ^[10] speculated that the biological and physicochemical attributes of the coffee rhizosphere could dictate their impact on Meloidogyne exigua suppression under field conditions. Thus, such suppressive soils caused about 83% M . exigua J 2 mortality and attained the highest yields of coffee beans. Thus, further plant–nematode–microbe interactions in suppressive soils require additional study to be better understood to enable novel insights for the best exploitation of suppressiveness. Westphal ^[5] reported a few methods to examine the biology of PPN soil suppressiveness. They mostly rely on comparing PPN reproduction in sterilized vs. non-sterilized soils. A drawback in this approach is that the growth parameters of plants are usually better in sterilized soil, which impacts the PPN activities and other biologicals as well. Therefore, it may bias the results ^[11]. While culture-independent methods on the related microbiome have given a better understanding of the functional potential of many PPN suppressive BCAs, culture-dependent techniques enabled the use of some microbial groups in specific suppressive soils ^[7]. Both approaches should be timely and adequately used to adjust recycling of the relevant microbiome in their host populations and expanded long-term PPN suppression in other soils.

Using BCAs is not an easy or routine task, but should be based on accurate, complementary data and a good conception of the possible involved factors. Therefore, sampling and primary tests are prerequisites to obtain the data on the related factors for effective IPM. Biological suppression may be assessed by comparing nematode reproduction in both untreated and treated soils with a proper biocide or heat to eliminate BCAs ^[11]. This test may take 1–3 months as targeted reproduction of PPNs is valued after at least one nematode generation. To shorten this period, survival of only free-living stages of the concerned PPNs may be assessed after several days in the untreated and treated soils. This alternative test offers rapid conclusions but, as such, is limited to measuring the effect of only BCAs on soil or migratory stages of PPNs. In the latter tests, other BCAs specialized in parasitizing PPN eggs and/or nematode-sedentary stages are mistakenly ignored. Furthermore, a PPN species not present in the field soil is preferably utilized in both tests to determine the level of biosuppression to avert the confusing impact of native nematodes, e.g., a host-specific parasite cannot be avoided. For instance, using the reniform nematode, Rotylenchulus reniformis , to evaluate its biosuppression in the sting nematode Belonolaimus longicaudatus -infested soil cannot detect a species-specific BCA, e.g., Candidatus Pasteuria usage, which is specific to parasitizing B. longicaudatus ^[12]. Mixing a small amount of the field soil into disinfested soil may resolve the issue. In this case, B. longicaudatus is conveyed with the field soil, and so other target PPNs can be added to the soil with few influences. Notwithstanding the utility of endemic B. longicaudatus to detect species-specific antagonists, the BCAs conveyed with the soil should have enough time to multiply to suppressive levels. The test does not negate that biocontrol of PPNs using an introduced BCA may not be as effective in various settings as that of indigenous BCA, due to ecological validity ^[13]. Eventually, relevant bioassays that validate PPN suppression in a specific agroecosystem should be carried out for the best BCA–PPN host matching.

3. Botanicals as Bionematicides

During their growth, antagonistic cultivated plants produce antihelminthic compounds that act as antagonists to the nematodes via various modes of action ^[14]. The nematostatic or nematicide compounds in the plant organs may be freed into the soil or operate within the plant to act as nematode traps or show unfavorable responses to PPNs. The broad conception of these plants may include different groups that can adversely affect various PPN populations, but poor and non-hosts will better be addressed separately ^[15] hereafter in more detail.

Using the relevant compounds via extraction from the plants or incorporating plant parts into the soil is another and more common tactic for PPN control than using the entire plants. These materials are mainly extracted or formed from antagonistic plants. They may be grouped under various terms, such as natural compounds, organic acids, essential oils (EOs), and plant extracts and compounds. In contrast, not all of these groups are exclusively related to plants. For instance, acetic acid is produced as secondary plant metabolites ^[16] or as culture filtrates of the bacterium, Lactobacillus brevis , strain WiKim0069 ^[17]. This acid can damage the cuticle of RKN J 2, vacuolize the cytoplasm, and degrade the nuclei, causing death ^[17]. Numerous organic acids, such as amino, propionic, formic, and butyric acids, can exert toxic effects on PPN species ^[18]. They are formed via microbial decomposition of other compounds in the soil, mostly those related to plant materials/residues, but may also result from metabolites formed by soil organisms. Others, such as sesquiterpene heptalic acid produced by the fungus, Trichoderma viride ^[19], and hydroxamic acids from the grass, Secale cereale ^[20], have proved effective against important PPN species.

Sikora et al. ^[21] suggested that antagonistic plants are very attractive tools for PPN control, but there are potentially new ones that could also be identified. Moreover, techniques should be sought for efficient and multi-purpose applications. Other merits of antagonistic plants are their effective operation in upgrading the soil characteristics. They are used as organic matter and green cover to raise soil quality ^[22]. Specific groups of antagonistic plants may possess additional merits. A striking example is to boost the activity of biocontrol agents against PPN in addition to their direct effect of reducing damage from pests. Contrary to the bacteria associated with soybean roots, the rhizobacteria isolated from the roots of antagonistic plant species Ricinus communis , Mucuna deeringiana , and Canavalia ensiformis could significantly decrease both Meloidogyne incognita and Heterodera glycines population densities on roots of soybean plants. Hence, Grubišić et al. ^[14] speculated that these plants may retain a selective action within each pest class as they possess multiple mechanisms with a wide spectrum. Additionally, these antagonists, related to legumes, can fix the atmospheric nitrogen, which boosts soil fertility.

More research is direly needed to determine the optimum conditions for these bionematicides in general. To optimize PPN control, their incorporation into the soil should target nematode-life stages and species that are most vulnerable. Variables, such as edaphic factors, tillage systems, proper planting date, favorable plant species, and suitable growth stage, should be examined to be best tailored for PPN control. Notwithstanding the nematicidal activity of brassicas cover crops to suppress PPN populations in soil, they may not provide consistent efficacy. Dutta et al. ^[23] stressed that temperatures may be too high for such plants to adequately show their nematicidal activities under greenhouse conditions.

4. Other Methods of PPN Management

The broad concept of soil amendments is to use not only plant materials as a cover crop, compost, seed meal, and green manure, but also to mix them with other components. Contrary to the above-mentioned botanicals, they may include, for instance, various animal manures and/or nutrient salts to form different varieties of amendments. These additions are mostly organic matter and have been used in multi-purpose agricultural practices. They can suppress the population levels of many pathogens, pests, and weeds, enrich soil fertility, boost soil structure, increase communities of beneficial organisms, and/or induce systemic resistance of plant species ^[23]. Organic amendment herein refers to organic material brought from outside to the inside of the soil, e.g., industrial waste products or processing residues. This differs from the above-mentioned botanicals, which were added as fresh crop residue or grown in the rotation, e.g., break, cover, trap, antagonistic or green manure crops. Usually, merging large amounts of such organic material into the soil will reduce PPN densities. These may include many materials, such as oil cakes, sawdust, coffee husks, crustacean skeletons, chicken manure, paper waste, and crop residues, which showed various degrees of PPN control ^[15]. This action was mostly associated with corresponding increases in crop yields.

Moreover, an amendment that works well in soil with specific edaphic and biological factors may not work at all in another soil. Optimizing the PPN control efficacy relies on its compounds’ compositions, quality, and quantity of its associated and interacting microbiome, and its ability to break down these compounds into elements that are suitable for plant growth and/or harmful to the nematodes. Fresh compost enriched with beneficial organisms and nutrients may show better efficacy against PPNs than aged compost. Abiotic factors, such as soil moisture and temperature, usually influence the microbiome and decomposition of these compounds. Soil amended with chicken manure and broccoli at ≥25 °C was superior to the same at 20 °C in reducing M. incognita galls on tomato roots ^[24]. Ntalli et al. ^[25] reviewed various soil amendments and their specific nematicidal activities. They categorized amendments as Brassicaceae and Asteraceae species (for cover-crop, biofumigation, rotation, and incorporation), biochars, composts, and vermicomposts (applied as recycling wastes), and other self-made products, such as canola or orange peel meals, dried leaves of Canabis sativa , and marigold or pennycress seed powder. Examples of safe strategies for applying various bionematicides or biocontrol methods against important nematode species are given    (Table 1). Nonetheless, some examples may need continuous improvement to the above-mentioned aspects to improve their efficacy and reliability.

Table 1. Examples of various biocontrol agents and strategies against important nematode species.

Using various composts as big sources of soil amendments should be further exploited. They could be manipulated via fermentation processes to make them enriched in the desired microbial species and PPN antagonistic compounds, such as phenolics and humic acids ^[26]. Composts can also enhance soil resident microbial antagonists, boost plant resistance or tolerance to various stresses, such as PPN infection, and change soil profiles to improper media for PPN reproduction. These gains should be optimized to improve PPN control by grasping the related edaphic factors as well. Eventually, their processes and components should be employed to obtain the desired PPN-suppressive soils.

Other treatments may be used when relevant factors and economic feasibility permit. For high cash crops, heating the soil can effectively manage RKN in protected cultivation ^[27]. Soil solarization could be effective against PPNs. Tarping the soil surface, especially in sunny regions, with transparent plastic sheets will raise soil temperatures enough to kill many pests and pathogens ^[28]. Solarization is more effective against PPNs in contained raised beds for cultivation in warm regions. Kokalis-Burelle et al. ^[29] found that the number of RKN galls on roots of sunflowers, snapdragon, and larkspur were less in steam-treated soil than in solarization alone. Steam treatment was as effective as methyl bromide in controlling M . arenaria . They concluded that soil steaming followed by solarization is so effective that it can be a safe alternative to chemical nematicides ^[29].

Biodisinfestation or biosolarization, that is, using soil amendments before solarization, could enhance the pest and pathogen suppression via rapid generation of harmful
compounds, such as acetic and butyric acids, ultraviolet radiation, and lack of oxygen, due to microbial anaerobiosis [27]. However, lethal temperature and related duration may vary from one pathogen species to another [87]. Thus, sustained low PPN populations were sometimes not affected by fairly high temperatures (45 C). In these cases, lasting PPN populations at deeper depths away from the sun could recolonize and infect the plant roots. Ozonated water, O3wat, was reported to control M. incognita likely via modulated antioxidant systems without phytotoxicity. Tomato plants treated with O3wat after or before M. incognita inoculation showed a root galling index (on a scale of 0–10) of 1.9 or 1.6, respectively, compared to 3.9 in the check [89]. As it degrades to water in a short time, O3wat could suppress RKN populations early in the growing season without adverse effects.

5.2. Advanced Methods

Table 2. Examples of bionematicidal product costs and used rates as compared to chemical nematicides in Egypt.

6. Conclusions