6. Evidence of hyperparasitic interactions
Studies of hyperparasitic interactions between fungi and their hosts
have been observed both in the field and by microscopy (Kim and
Vujanovic, 2018; Moore et al., 2020; Smith et al., 2008).
However, in most cases, the antagonistic activity of the hyperparasite
is not evident in the field, and the exact interactions may only be
revealed under laboratory conditions, when the cultivation of the
hyperparasite is possible or when infected primary and/or secondary
hosts can be reared.
The associations of hyperparasites and their hosts can be visualized by
molecular techniques that employ expression of fluorescent proteins
(Hasan et al., 2022). For example, the gene-encoding green
fluorescent protein (GFP) was expressed in Trichoderma species,
which helped to elucidate their interactions with Pythium
ultimum, the invasion of the hyphae and sclerotia of Rhizoctonia
solani, and the penetration of the plant-parasitic nematode Globodera pallida (Contina et al., 2017; Lu et al.,
2004; Sarrocco et al., 2006). Also, Németh et al. (2019)
used a GFP marker to visualize the life history strategy of Ampelomyces quisqualis.
Hyperparasitic interactions may be assumed if the parasite causes
distinctive morphological or physiological alterations of the primary
parasite, with the latter showing signs of phenotypic changes, such as
deformation of cells, growth impairment, and changes in color (Gams et al., 2004; Jeffries, 1995; Zheng et al., 2017). For
example, urediniospores of Puccinia striiformis f. sp. tritici collapse and lose viability after being colonized by
hyphae of Alternaria alternata and Cladosporium cladosporioides (Zhan et al., 2014; Zheng et al., 2017).
Parasitism may also be assumed when parasites affect the reproductive
rate of the hosts, e.g., by decreasing levels of sporulation of fungal
hosts. This has been observed for hyperparasites of black mildews,
powdery mildews, and rusts and smuts (Bermúdez-Cova et al., 2022;
Legler et al., 2016; Zhan et al., 2014; Zheng et
al., 2017). The incapability of fungi growing on parasites to be
cultured on axenic media, i.e., without their hosts, also serves as an
indication that they are obligate hyperparasites (Jeffries, 1995).