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 cinerea, Fusarium 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.