Rust fungi (Uredinales) are one of the largest groups in the Basidiomycota, comprising about 5000–6000 species found on a wide range of hosts, including ferns, gymnosperms, and mono- and dicotyledonous angiosperms (Alexopoulos et al. 1996). Diseases such as coffee leaf rust, Hemileia vastatrix, wheat stem rust, Puccinia graminis, Melampsora leaf rusts of Salicaceae (Populus and Salix) and Cronartium stem rusts of hard pines are causing enormous losses and often making it necessary to replace susceptible crops entirely with non-host species (Littlefield 1981).
Smuts primarily affect grasses viz corn (maize), wheat, sugarcane, barley, oats, forage grasses and sorghum (Feldbru¨gge et al. 2013). A smut is characterized by spores that accumulate in soot-like masses called sori, which are formed within blisters in seeds, leaves, stems, flower parts, and bulbs (Laurie et al. 2012). The sori usually break up into a black powder that is readily dispersed by the wind. Many smut fungi enter embryos or seedling plants, then develop systemically, and appear externally only when the plants are nearing maturity (Liu et al. 2017a). Currently, the most widely used control method for sugarcane smut disease is the breeding of resistant cultivars (Shen 2002; Wada 2003; Croft et al. 2008; Lwin et al. 2012; Shen et al. 2014). However, its development is constrained by long breeding processes, high costs, and the availability of smut resistant parental lines. Disease attributed to smut fungi could also be controlled by soaking seed canes with chemical fungicides (Olufolaji 1993; Bhuiyan et al. 2012). Another approach is using plant or fungal extracts that inhibit smut pathogen germination and growth (Lal et al. 2009). A large number of fungi have been identified as hyperparasites of rust and smut fungi, which are being used as biocontrol agents worldwide (Gowdu and Balasubramanian 1988; Kranz 1981; Feldbru¨gge et al. 2013).
Various studies support the ability of certain fungi to control the growth of smuts and rusts. The mechanisms through which biocontrol agents act are antibiosis, secretion of metabolites that are toxic, lytic enzymes, parasitism and competition for nutrients. Figure 3 shows the different mechanisms of antagonistic fungal species action. Biological approaches are gaining popularity, including the use of microbial antagonists (Eckert and Ogawa 1988). Cladosporium species co-exist with rust sori, and some are believed to be invariably hyperparasites of Uredinales
(Moricca et al. 1999). Cladosporium uredinicola is a common necrotrophic hyperparasite that can destroy rust hyphae and causes coagulation and disintegration of the cell cytoplasm of Puccinia cestri (Spegazzini 1912), Puccinia (Ellis 1976), Cronartium quercuum (Morgan-Jones and McKemy 1990), Puccinia violae (Traquair et al. 1984) and Puccinia horiana (Srivastava et al. 1985). Moreover, C. uredinophilum was also reported to colonize and destroy Uredo cyclotrauma propagules in Paraguay (Spegazzini 1912). Steyaert (1930) also described C. hemileiae as an effective hyperparasite of coffee rust fungus, Hemileia vastatrix, in Zaire (Democratic Republic of Congo). Powell
(1971) reported that C. gallicola in galls of Cronartium comandrae on Pinus contorta var. latifolia is parasitic on aeciospores. Hyphae of C. gallicola penetrate into the aeciospores of pine gall rust, Endocronartium harknessii (Sutton 1973). Tsuneda and Hiratsuka (1979) investigated C. gallicola and found that it parasitized E. harknessii by both simple contact—disintegrating the cell walls of the spores—and by actual penetration of the spore walls, with
or without the formation of appressoria, causing the coagulation and disappearance of the host cytoplasm. Hulea (1939) and Rayss (1943) documented a similar phenomenon where C. aecidiicola, a common hyperparasite of rusts in Europe and in the Mediterranean area, parasitized E. harknessii on Pinus spp. in California (Byler et al. 1972). Keener (1954) stated that this hyperparasite also drastically parasitized aecia of Puccinia conspicua in Arizona and urediniospores of Melampsora medusae under storage conditions (Sharma and Heather 1980). Moreover, Srivastava et al. (1985) also documented that Puccinia horiana was often regulated by Cladosporium sphaerospermum and C. tenuissimum. They were also detected from aeciospores of the two-needle pine stem rust Cronartium flaccidum (Moricca et al. 1999). Other groups of fungi aside from Cladosporium were also reported to act as biocontrol agents. The entomopathogenic and mycoparasitic fungus Lecanicillium lecanii is also known to attack coffee leaf rust, Hemileia vastatrix (Jackson et al. 1997).
Not many commercial biofungicides for rust and smuts based on antagonistic fungi are currently available. Mahmud and Hossain (2016) showed that the BAU-biofungicide (2%) (Trichoderma based preparation) significantly affected the mycelial growth of Ustilaginoidea virens in an in-vitro test, but this observation remains to be confirmed in greenhouse and field trials.
Kranz (1981) documented more than 80 species of fungi from over 50 genera reported as hyperparasites of rusts. However, this number might be an overestimate due to some taxa being synonyms. Even though this large number of antagonistic fungi on rusts and smuts has been reported, few commercially, improved biofungicides are available for practical application. As in other applications of biocontrol agents, product formulation is the most critical step of the entire development process (Janisiewicz and Jeffers 1997). The next few years will likely see the increased application of biocontrol agents in agriculture, with particular emphasis on the use of mixtures of antagonists on the same plant organ. This approach may lead to a wider spectrum of activity of the biological treatment or an increase in either the efficacy or consistency of the biological treatment. Furthermore, collaborative work of academic, federal and private sector scientists is necessary to develop more effective and consistent biofungicides.