More than 80 species and approximately 30 genera of fungi can parasitize rust fungi (Pucciniomycetes: Pucciniales) and are, mostly asexual forms of Ascomycota (Gams et al ., 2004; Hawksworth, 1981; Kranz, 1981; Leinhos and Buchenauer, 1992; Zhan et al ., 2014; Zheng et al ., 2017). In the genus Cladosporium , C. aecidiicola ,C. cladosporioides, C. pseudocladosporioides, C. sphaerospermum ,C. tenuissimum, and C. uredinicola have been reported as hyperparasites of rust fungi (Keener, 1954; Mendgen, 1981; Moriccaet al ., 1999; Sharma and Heather, 1978; Srivastava et al ., 1985; Sun et al ., 2019; Torres et al ., 2017; Traquairet al ., 1984; Tsuneda and Hiratsuka, 1979; Vandermeer et al ., 2009; Wang et al ., 2016; Zhan et al ., 2014).Cladosporium species are in close contact with the cells of the rust fungus, through formation of appressoria and penetration of the host cells by mechanical force or through the production of lytic enzymes (Assante et al ., 2004; Moricca et al ., 2001; Nasini et al ., 2004).
Species of the genus Tuberculina (Pucciniomycetes: Helicobasidiales) are known only to be parasitic on rust fungi (in their asexual stage), living in association with more than 150 host species from at least 15 genera (Hawksworth, 1981; Lutz et al ., 2004). The most common species are T. maxima and T. persicina , reported from species of Cronartium and Gymnosporangium , respectively (Hawksworth, 1981; Hubert, 1935). Tuberculinaspecies have an alternating life cycle (Lutz et al ., 2004) with morphologically and ecologically distinct sexual and asexual stages, which were formerly classified into different genera:Helicobasidium for the sexual stage and Tuberculina for the asexual stage.
In their asexual stage, Tuberculina species produce lilac to violet sporodochia-like structures growing on the sori of rust fungi. Cytoplasmic contacts between host and parasite are facilitated by micrometer–fusion pores, structures that are unique among Basidiomycota (Bauer et al ., 2004). In the sexual stage, these species are phytopathogens that form purplish crust-like sporocarps on living and dead plant material, causing violet root rot on a multitude of plant host species.
Quasiramularia phakopsoricola (Ustilaginomycetes, Basidiomycota) is a mycoparasite on the rust Phakopsora ampelopsidis and represents the only known mycoparasitic member among Ustilaginomycotina (Kolařík et al. , 2021). This hyperparasite resembles the hyphomycetous morphology of Ramularia species (Dothideomycetes, Ascomycota), and its affinity to Basidiomycota was only proven by phylogenetic analyses. Sexual reproduction in this species is not known, and the host-parasite interaction mechanism remains to be investigated.
The most common hyperparasite of rust fungi is the pycnidial fungusSphaerellopsis filum (Dothideomycetes: Pleosporales). This is a biotrophic hyperparasite that grows mostly in the uredinia of its host (Gams et al ., 2004; Keener, 1934). Through the production of enzymes, it is able to penetrate urediniospores to inhibit their germination (Carling et al ., 1976; Leinhos and Buchenauer, 1992; Stähle and Kranz, 1984). Sphaerellopsis filum has a broad host range among rust fungi; and has been documented from over 360 species in 30 genera (Leinhos and Buchenauer, 1992).
Akanthomyces lecanii and Aphanocladium album(Sordariomycetes: Hypocreales) are necrotrophic hyperparasites that penetrate and destroy spores of Puccinia graminis (Gams et al ., 2004; Leinhos and Buchenauer, 1992). The infection of urediniospores by A. lecanii induces precocious teliospore formation, which may be a self-defense mechanism of the rust fungus against the hyperparasite (Koç and Défago, 1983). Species ofAcremonium , Fusarium, Simplicillium (Sordariomycetes: Hypocreales), Alternaria (Dothideomycetes: Pleosporales), andVerticillium have also been reported as hyperparasites (Buchenauer and Leinhos, 1982; Gams, 1975; Wollenweber, 1934; Zhenget al ., 2017). Many other potential parasites of rust fungi are cited by Hawksworth (1981), Gowdu and Balasubramanian (1988), Leinhos and Buchenauer (1992), and Gams et al . (2004).