Plant–parasitic nematodes (PPNs) in soil can be prey for several pathogens, such as viruses, -bacteria, and fungi. Many groups of these pathogens can be utilized in the biological control of nematodes (Rilrron, 1977).

However, using new control methods instead of synthetic chemicals is necessary to improve sustainable agriculture (Aguilar-Marcelino et al., 2020a,b, 2021; Al-Ani et al., 2020a, 2021a,b; Sharma et al., 2020; Singh et al., 2021). Many plant pathogens, such as Alternaria spp. (Garganese et al., 2018), Aspergillus spp. (Attitalla et al., 2010a,b), and Fusarium spp. (Mohammed and Al-Ani, 2021), caused a high reduction in plant growth and yield. The utilization of natural factors showed high efficacy in conferring protection for plants from plant pathogens and pests. Plant growth promoting rhizobacteria (PGPR) biocontrol agents showed the ability to control several plant pathogens (Al-Ani, 2006, 2017a, 2018a,b; Al-Ani and Al-Ani, 2011; Mohammed et al., 2011, 2014; Al-Ani et al., 2020b; Soumare et al., 2021). Trichoderma is a more interesting genus used in biological control that has shown efficacy in the management of several plant diseases (Al-Ani et al., 2013a, 2018; Al-Ani and Albaayit, 2018a,b; Al-Ani, 2019a,b; Al-Ani and Mohammed, 2020) and has been detected as act endophyte in plants (Al-Ani, 2019c,d,e).

Non-pathogenic fungi and entomopathogenic fungi controlling plant disease and pests (Al-Ani et al., 2018; Al-Ani, 2019c,f; Gupta et al., 2022), have the ability to manage some plant diseases and play a role in sustainable agriculture by enhancing plant vigor (Al-Ani and Salleh, 2010; Al-Ani et al., 2013b; Al-Ani, 2017b, 2019d,e; Al-Ani and Furtado, 2020; Kisaakye et al., 2022). In addition, many natural compounds and plant extracts are helpful in controlling plant diseases and pests (Al-Ani et al., 2012; Mohammed et al., 2012, 2013; Adetunji et al., 2019; Garganese et al., 2019; Jatoi et al., 2020). NF are used in the control of parasitic nematodes as bionematicides by parasitism, and produce toxins to kill nematodes, as well as induce defense and resistance mechanisms in plants against parasite nematodes (Abd-Elgawad and Askary, 2018; Sarker et al., 2020; Comans-Pérez et al., 2021; Girardi et al., 2022). NF as biological control factors are the best method to use in sustainable agriculture. NF belong to most groups of fungal taxa, such as Oomycota, Zygomycota, Ascomycota, Pleurotaceae (Basidiomycota), and Chytridiomycetes (Gams and Zare, 2003; Wijayawardene et al., 2020).

Many NF have not yet been discovered, and around 6,000–8,000 species are waiting for identification (Li et al., 2000; McInnes, 2003; Yang et al., 2012). NF inhabit the soil and rhizosphere (Liu et al., 2009) and have been detected in several soils but not in soil from extreme environments, such as high salt concentrations and high temperatures (Yang et al., 2020). NF are divided into five types: (A) nematode-trapping fungi, (B) endoparasitic fungi, (C) fungi that secrete toxins affecting nematodes, (D) egg-parasitic fungi, and fungi that induce resistance and defenses in plants, which then influence the activity of or kill PPNs (Swe et al., 2011; Maia Filho et al., 2013).

The secondary metabolites of some NF shown high efficacy in controlling parasitic nematodes (Castañeda-Ramírez et al., 2020; Seong et al., 2021). In the present review, we discuss the strategy of NF in the control of plant-parasitic nematodes and their activity in sustainable agriculture.

Soil NF are a heterologous group that acts as a natural enemy of parasitic nematodes. These fungi use nematode biomass as a source of carbon, nitrogen, and other important elements (Siddiqui and Mahmood, 1996); some of them are obligate parasites of nematodes, but the majority are facultative saprophytes (Lopez-Llorca et al., 2007).

These NF have been studied for their use as a biological control against PPNs. Biological control of phytonematodes can be defined as the decrease in nematode populations by the action of living organisms other than those naturally found in the host plant by the manipulation of the environment or by the introduction of antagonist organisms (Kim, 2015). To this day, more than 200 species of taxonomically diverse fungi have shown the ability to attack living nematodes in their different stages: juvenile, adults, and eggs (Nordbring-Hertz et al., 2006).

The morphology of nematodes presents two different barriers against fungal infection. The first is the eggshell, which in root-knot and cyst nematodes consists of three layers: the outer vitelline composed mainly of proteins, the chitin layer, and the inner lipoprotein layer; and the second barrier, the cuticle (Figure 1). The thickness of these barriers varies considerably depending on the nematode genus (Morton et al., 2004). The types of mechanisms used by NF to infect nematodes can be divided into parasitism, toxic compounds, and enzymes (Figure 2).

Nematophagous fungi are more helpful for the biological control of PPNs compared to other organisms, such as bacteria and viruses. These NF are available in the environment of prey nematodes. The importance of NF can be divided into two types: direct and indirect effects. Direct effects indicate the capability of NF to directly affect nematodes by parasitising adults, juveniles, and eggs, as well as producing toxins or secondary metabolites causing nematode immobility. Many NF use the mechanisms mentioned previously. For indirect effects, this mechanism can happen by inducing both plant defenses (Lopez-Llorca et al., 2010), and plant resistance in monocotyledon and dicotyledon (Bordallo et al., 2002), that affect the activity of PPNs, such as laying eggs, hatching eggs, completing the life cycle from juveniles to adults, and immobilization. Two nematophagous fungi Arthrobotrys oligospora and Verticillium chlamydosporium colonized the plants both of barley and tomato (Bordallo et al., 2002). Endophytic Fusarium oxysporum showed the capability to reduce the population of PPNs Meloidogyne sp. after it was used to treat bananas (Waweru et al., 2014). Some biocontrol fungi, such as Trichoderma, can be useful in reducing the pathogenicity activity of nematodes by affecting juveniles (an important stage for causing plant disease) and eggs. Trichoderma asperellum T-16 reduced the densities of juveniles (second-stage J2s) in roots by about 80%, but T. brevicompactum T-3 could suppress the production of eggs by around 86% (Affokpon et al., 2011).

Plant–parasitic nematodes are a major cause of losses in world agriculture, resulting in yield and monetary losses. Nematodes can grow undetected by the farmer due to their microscopic size, underground habitat, and non-specific plant infection symptoms (Kim, 2015). Much damage to crops goes unreported or is often classified with other causes, such as fungal attacks, hydric stress, nutritional deficiencies, or other soil factors (Abd-Elgawad and Askary, 2018).

Chemical nematocides are the most traditional option for the management of PPNs, but their application is increasingly being re-evaluated because of their multiple environmental and health hazards, in addition to their low availability and high cost (Degenkolb and Vilcinskas, 2016a,b). Another major disadvantage of the frequent use of these chemicals is that they can result in the generation of resistant nematode races, which can make their control even more difficult (Abd-Elgawad and Askary, 2018).

Because NF can actively feed on and are the natural antagonist of PPNs. This trend includes the study of these fungi in their application form, shelf life, culture, mass production, effectiveness with other biotic and abiotic factors, and crop management techniques (Kim, 2015).

Bioproducts with these NF in their formulation present several benefits for more sustainable agriculture against chemical nematicides, such as easy application, environment safety, do not affect the soil biota, and do not leave residues in harvested products. However, as a living system, there are several considerations to note when developing a commercial bionematicidal product. To accomplish effective and reproducible biological control, this study is important for the determination of both the biotic and abiotic factors that affect the biocontrol agent and the target parasite (Figure 4). The fungi to be used must be able to grow well in the field to be treated, considering the influence of chemical, physical, and other biological factors in the soil that act like fungistatic compounds, in addition to the fact that these factors can be difficult to predict due to crop rotations (Yang et al., 2007).

Therefore, the use of new technology has been incorporated into biopesticide production. One example is the use of real-time quantitative PCR technology to quantify and track the biocontrol agent after it has been applied to the soil. Similarly, genetic modification of biocontrol agents can improve their efficacy by achieving overexpression of genes involved in pathogenicity or nematocidal activity (Zhang et al., 2020a,b). Genetic modification approaches are utilized for enhancing the virulence, aggression against nematodes, UV protectants, expression of heat shock factors, immune modulators, and cuticle degrading enzymes.

There are two general techniques for using NF as a biological control agent. One technique is the addition of large amounts of fungi to the soil or as an endophytic organism of the plant by coating seeds to favor the colonization of its rhizosphere. The fungus can establish itself before the nematodes are attracted to the plant roots (Nordbring-Hertz et al., 2006). The second technique is to improve the bionematicide formulation with the complementary use of biocontrol agents nematophagous fungus the improve the growth, adaptability, and efficiency of NF as an integrated pest management technique (Yang et al., 2007). In this situation, the integrated use of a fungus as a biocontrol agent in addition to a lower dose of chemical pesticide or plant product can give effective results if the components are compatible (Kim, 2015).

There have been various formulations to maximize the action of the biopesticide. A study of the fungus T. viride in combined application with the chemical nematicide carbofuran has shown an increase in plant height, root length, and decreased nematode M. graminicola population in rice crops (Pankaj et al., 2015).

Similarly, a formulation of the ovicidal fungus P. lilacinus added to the plant product neem cake shows egg parasitism of the nematode N. incognita and plant growth in tomatoes (Zaki and Maqbool, 1992). Other formulations include the use of the phytohormone abscisic acid (ABA), which enhances plant defense and increases the nematode-trapping capability of D. stenobrocha, a constricting ring-forming fungus (Xu et al., 2011). Different studies have also demonstrated an effective integrated pest management technique for the PPNs with bacteria P. fluorescens or a combination of several species of fungi (Abd-Elgawad and Askary, 2018).

The interaction between fungi and nematodes is interesting, especially the use of NF as an alternative to synthetic chemicals that are used in the manufacture of nematocides. In recent years, techniques have been developed for genome sequencing and transcriptome analysis, as well as for analysis techniques for detecting chemicals at the nano level. We have a lot of information about the relationship between NF and nematodes that comprises enzymes and secondary metabolites as toxins. This antagonistic relationship depends on creating a special structure to capture the host and produce a toxin. Information on the interactions can be supplied through “-omics” data. The enhancement in the manufacture of bionematicides is depending on selecting aggressive isolates of NF by determining the virulence factors to a molecular level for isolates of NF. Efficiently obtaining bionematicides is a target and requirement for all researchers in the field of agriculture sustainability. Some information is still lacking, depending on the factor of pathogenicity.

Some enzymes, such as serine proteases, chitinases, and toxins, of NF are more interesting in the process of infection against parasitic nematodes through their role as virulence factors. The production of different enzymes in the process of infection of parasitic nematodes requires their penetration of diverse layers of cuticle and eggshell. The success of some strains of NF indicates differences in host preference. Some NF, such as the genus Trichoderma, play an important role in sustainable agriculture. Finally, we consider the high utilization of NF in the control of PPNs as an alternative to synthetic chemicals, and they may be more useful in sustainable agriculture, reducing harmful chemical residues in the ecosystem.

All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.

This present mini review article was partially financed by the Proyectos Fiscales Instituto Nacional de Agricultural and Livestock Forestry Research, INIFAP (project number: 139335341).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.