8. Hyperparasitic fungi and biological control

Environmental and health concerns caused by the use of chemicals such as fungicides, nematicides, and pesticides have increased the need for alternative measures for the control of pathogens (Moosavi and Zare, 2020; Thambugala et al., 2020). Hyperparasitic fungi play a significant role in controlling pathogens, and they have been used as biological control agents for at least 70 years (Heydari and Pessarakli, 2010; Thambugala et al., 2020). Biocontrol agents represent an alternative to fungicides in disease control (Köhl et al., 2020). The use and utility of biocontrol agents, however, has had limited success (Savita and Sharma, 2019) and more work is needed to fully examine the most appropriate and beneficial applications of specific hyperparasites in biocontrol.
The fungi best studied for their use in biocontrol are species of the genus Trichoderma (Brotman et al., 2010; Harman et al., 2004; Motlagh and Samimi, 2013; Reino et al., 2008). Around 90% of fungal biocontrol agents belong to different strains of Trichoderma, and currently more than 60% of the effective bio-fungicides are obtained from species of this genus (Abbey et al., 2019; Hermosa et al., 2012). Moosavi and Zare (2020) stated that 25 species of Trichoderma have the potential of controlling more than 100 fungal pathogens worldwide. Out of these species, Trichoderma harzianum may be considered the most common and commercially developed biocontrol agent used for a wide range of plant-pathogenic fungi. Trichoderma species have an antagonistic behavior against bacteria, nematodes, and fungi by inhibiting growth and they may indirectly improve the growth and stress tolerance of the primary plant host (Kumar, 2013; Zhang et al., 2017).
Clonostachys rosea is a hyperparasitic fungus capable of invading various plant-pathogenic fungi, including Botrytis cinereaFusarium spp., Rhizoctonia solani, and Sclerotinia sclerotiorum (Barnett and Lilly, 1962; Cota et al., 2008; Jensen et al., 2000; Luongo et al., 2005; Rodríguez et al., 2011), with C. rosea strain 67-1 being highly efficient for biocontrol (Zhang et al., 2007; Ma et al., 2011; Sun et al., 2018). Hasan et al. (2022) showed that the GFP-marked C. rosea strain 67-1 exerts antagonistic activities against B. cinerea both in vitro and on tomato leaves. The hyperparasite is able to penetrate its host, absorb its nutrients, and eventually disintegrate all of its cells.
Ampelomyces quisqualis has been the subject of numerous investigations on biological control of powdery mildews for over 50 years and, along with species of Trichoderma, they are the most common biocontrol agents that have reached international markets (Falk et al., 1995a, 1995b; Kiss et al., 2004). Several cross-inoculation experiments, both in vitro and in the field (Angeli et al., 2012; Kiss et al., 2011; Legler et al., 2016; Liang et al., 2007; Németh et al., 2021), have shown that species of Ampelomyces are not strictly host specific. This has allowed for biocontrol agents composed of a single strain to be applied to a wide range of powdery mildew species (Németh et al., 2021).
A large number of crop plants are infected by parasitic nematodes (Savita and Sharma, 2019). They represent a major threat to crops worldwide, and due to the toxicity of nematicides, new control strategies against nematodes need to be developed (Poveda et al., 2020). Fungi have shown great potential as nematicidal biocontrol agents (Siddiqui and Mahmood, 1996). Important fungi used in biocontrol of nematodes are Pochonia chlamydosporia (Sordariomycetes: Hypocreales), Purpureocillium lilacinum (Sordariomycetes: Hypocreales), and Hyalorbilia oviparasitica (Orbiliomycetes: Orbiliales) (Lysek and Sterba, 1991). Species of Trichoderma are also currently being studied as biocontrol agents of parasitic nematodes.
The processes of commercialization and application of fungi as biocontrol of pests have been slow. This is mainly due to diverse fungal performances under variable environmental conditions in the field as well as their host specificity (Thambugala et al., 2020). The development of new formulations of biocontrol fungi with higher degrees of stability and survival is necessary to overcome this problem (Heydari and Pessarakli, 2010). Commercialization of biological control agents is expensive and involves many steps such as isolation in pure culture, the development of a suitable formulation, mass production, testing efficacy of the product, environmental safety matter assessment, among others (Janisiewicz and Korsten, 2002; Montesinos, 2003). Moreover, the cultivation of hyperparasites is not always possible and therefore the development of biocontrol products from these fungi remains challenging.