Plant-parasitic nematodes are parasites which cause severe damage to many economically important crops such as tomatoes, potatoes and wheat. For example, around US $80 billion of yield losses are caused annually by damage from plant root–knot nematodes, such as M. javanica and M. incognita (Li et al. 2007). Nematicidal chemicals that were once rather effective, such as methyl bromide, have ultimately been banned because they are broad-spectrum biocides that kill all life in the soil and contribute to the depletion of the ozone layer, thereby causing grave problems to the environment. Therefore, in recent years there have been great efforts in both academia and industry to find ecologically viable alternatives.
Nematophagous fungi are capable of controlling plant parasitic nematodes through antagonistic behaviour (Zaki and Siddiqui 1996). There are more than 700 species of nematophagous fungi, which are found in fungal taxa including Mucoromycota, Basidiomycota, Ascomycota and Chytridiomycota (Li et al. 2005; Degenkolb and Vilcinskas 2016). These nematophagous fungi are categorized into four groups according to their mode of parasitism: nematode-
trapping (otherwise known as predacious); nematode egg and female parasites; endoparasitic; and toxin-producing fungi (Li et al. 2005; Degenkolb and Vilcinskas 2016). Nematode–trapping fungi form specific trapping structures on hypha, such as adhesive knobs, constricting rings and adhesive networks; these three trapping devices can be categorized further into seven types: simple adhesive branches, unstalked adhesive knobs, stalked adhesive knobs, non-constricting rings, constricting rings, two dimensional networks and three-dimensional networks (Rubner 1996).
The constricting ring trap is the most sophisticated morphological adaptation, which can be found in fungi that are no accommodated in the genus Drechslerella (Baral et al. 2018). When a nematode enters the ring, the three cells swell, forming three sphaerical structures that trap and immobilize the nematode (Jansson and Lopez-Llorca 2004). Endoparasitic fungi attack nematodes orally or by penetration of spores or zoospores through the cuticles of the nematode host (Moosavi et al. 2011). After infection, the hyphae develop inside the nematode and digests its content. For example, the spores of Catenaria anguillulae are ingested by sedentary nematodes such as Heterodera spp. The spores germinate in the esophagus and the mycelia then digest the nematodes; 10–12 h after the infection, zoosporangia develop to release new zoospores (Mankau 1980). The motile zoospores are adapted by having positive tropisms toward nematodes (Kumar et al. 2017). Nematode egg parasitic fungi play a key role in infecting the eggs of nematodes on two levels. Some fungi directly infect the nematode eggs by penetrating the eggshell, while others indirectly affect the content of eggs, such as larvae or embryos (Jansson and Lopez-Llorca 2004). Recent studies found that Ijuhya vitellina forms hyphae from the infected egg shells of the cereal cyst nematode Heterodera filipjevi to develop into microsclerotia (Ashrafi et al. 2017a). Monocillium gamsii and M. bulbillosum are two nematode-associated fungi parasitic to eggs of H. filipjevi (Ashrafi et al. 2017b). The first record of dark septate endophytes with nematicidal effects was reported from the new genus Polyphilus, represented by two new species (Ashrafi et al. 2018). Actually Polyphilus spp. have been isolated from nematode eggs as well as from healthy plant material.
Several studies related to nematode parasitic fungi that are specific to economically important crops have been conducted. Cochliobolus sativus (on wheat and barley), Dendriphiopsis spp. (on tomato plants) and Drechmeria coniospora are some controlling agents for root knot disease caused by nematodes on wide variety of crops, especially tomatoes (Jansson et al. 1985). A combination of Trichoderma species and nematode-trapping fungi was most effective in controlling plant-parasitic nematodes through egg parasitism (Szabo 2014). Moreover, there are some fungi which are capable of controlling nematode diseases in animals (Zhang et al. 2007). For example, animals infected by plant-parasitic nematodes are fed with fungal mycelium containing chlamydospores of nematode trapping fungi, e.g. Duddingtonia flagrans (Zhang et al. 2007). When fed to the animals. these spores produce traps in the faeces and surrounding grasses to capture newly hatched nematode juveniles (Zhang et al. 2007). Purpureocillium lilacinum is capable of controlling root–knot nematodes such as M. javanica and M. incognita on tomato, eggplant and other vegetable crops (Moosavi 2014). Some studies have reported the antagonistic behaviour of Arthrobotrys dactyloides against root knot nematodes on tomato plants, but other experiments with Metacordyceps chlamydosporia did not significantly reduce nematode population (Nordbring-Hertz et al. 2011).
Cochliobolus sativus was also reported to be an effective biological control agent in controlling nematodes in Botswana (Mubyana-John and Wright 2011). The combination of Purpureocillium lilacinum (previously referred to as “Paecilomyces lilacinus”) and Dactylella lysipaga was experimentally proved to be antagonistic to the root–knot nematode Meloidogyne javanica as well as the cereal cyst nematodes Heterodera avenae and Radopholus similis on tomato barley and banana plants (Zhang et al. 2014a, b). In another study, the combination of Purpureocillium lilacinum and Monacrosporium lysipagum was shown to be antagonistic to Meloidogyne javanica, the cereal cyst nematode (Zhang et al. 2014a, b).
Few studies conducted thus far have proven the efficacy of nematode parasitic fungi; however, individually these
fungi do not possess all the desirable characters required to serve as high potential nematode control agents. Thus combinations of nematophagous fungi can be more effective, as these combinations are capable of being parasitic in all stages of the nematode life cycle. Therefore, it is necessary to develop new techniques to facilitate research on nematode parasitic fungi, especially for tracing high potential strains in the environment. More studies are needed to improve and introduce more efficient strategies to produce biological control agents without harming nontargeted nematode species.
Liquid fermentation and solid fermentation are two methods of mass producing nematophagous fungi. Solid culturing is preferable for fungi that cannot produce spores in liquids (Zhang et al. 2014a, b). However, liquid culturing is widely used for the mass production of the spores and mycelium of targeted fungi (Zhang et al. 2014a, b). In fact, the combination of these two methods enhances the effectiveness of the mass production of fungi, as the liquid method can be used for producing mycelia and the solid method for producing conidia. The formulation of the fungal production is important in its commercialization as a bio control agent. Formulations are powders, wettable powders, emulsions, oil solutions, granular formulations, blending agents and microcapsules (Liu and Li 2004). Microencapsulation is a new method of commercializing bio control fungi (Patel et al. 2011). The latter researchers developed a novel capsule system using Hirsutella rhossiliensis. Jin and Custis (2011) also introduced a modified method for microencapsulation of Trichoderma conidia using sugar, which was then developed as a sprayable formulation.
Toxin-producing fungi secrete nematicidal metabolites to attack and immobilise nematodes before the development of hyphae inside the nematode (Degenkolb and Vilcinskas 2016). For example, Purpureocillium lilacinum produces acetic acid to immobilize juvenile parasitic nematodes (Djian et al. 1991). According to previous studies, more than 270 toxin-producing fungi have been recorded, including 230 nematicidal toxic compounds (Zhang et al. 2011a; Li et al. 2007). Recent examples include the report on the new genus and species Pseudobambusicola thailandica, which can control nematodes using its secondary metabolites, such as monocerin and deoxyphomalone (Rupcic et al. 2018). Linoleic acid is one of the nematicidal compounds that can be isolated from many fungi, including Arthrobotrys species, in which the production of this compound increases with the number of traps (Anke et al. 1995). Pleurotus pulmonarius and Hericium coralloides are two basidiomycetes that exhibit strong nematicidal effect against Caenorhabditis elegans. p-Anisaldehyde (46) and other aromatic metabolites, as well as fatty acids, were identified as active principles (Stadler et al. 1994).
Metabolites with moderate nematicidal activity have been recently reported from a Sanghuangporus sp. collected in Kenya. In addition to 3, 14′-bihispidinyl and hispidin and the new dcerivative phelligridin L (49), with moderate effects on Caenorhabditis elegans (Chepkirui et al. 2018). Ophiotine (45), a depsipeptide from a species of the Phaeosphariaceae isolated from nemtatode eggs, was reported to have a moderate nematicidal effect on Heterodera filipjevi (Helaly et al. 2018a). Chaetomium globosum produces flavipin, which inhibits egg hatching and juvenile mobility of the root-knot nematode (Meloidogyne incognita) and the hatching of soybean cysts (Heterodera glycines) (Nitao et al. 2002). Chaetoglobosin A and its derivate 19-O-acetylchaetoglobosin A are two other recently demonstrated chemical compounds isolated from Ijuhya vitellina, a parasitite of the eggs of Heterodera filipjevi (Ashrafi et al. 2017a, b). However, the most important fungal nematicides found to date are (a) PF-1022A, a precursor of the semisynthetic drug emodepside (48), which is used in veterinary medicine (Jeschke et al. 2005); and (b) the cyclopeptide omphalotin A (47) from cultures of the basidiomycete genus Omphalotus, which was also developed as a nematicide against Meloidogyne, but did not yet make it to the market because of unfavourable costs of goods (Sandargo et al. 2019a).
Many studies have shown the parasitic efficiency of nematode parasitic fungi, but it is necessary to develop IPM strategies to optimize the ability nematophagous fungi to colonize plant roots. High virulence strains and formulations are important for the development of more efficient commercial products. The utilization of the secondary metabolites of fungi as nematicides is not satisfactory at the commercial level as there are few bionematicides available in the market. On the other hand, integrated nematode management strategies can be implemented to improve the effectiveness of nematicidal action and minimize the use of chemical nematicides to the soil. Future bio products should be targeted not only for one species of nematode, but to disease complexes in concert with other pathogens like fungi, bacteria and viruses.