Smut fungi are a species-rich group, which are typically plant parasites that occur in a variety of habitats (Begerow et al. 2014, Vánky 2012). Many are rare, with one third found only once. The majority of smut fungi produce blackish spore masses in different organs of plants. Some species produce a light coloured spore mass in the anthers of plants or white to yellow spots in the leaves or galls of various plants. Many smut fungi are undescribed and many cryptic species and species complexes exist (e.
g. Kruse et al. 2017a, Piątek et al. 2013). Correct species identification of smut fungi is important for sound plant health management and effective biosecurity (Choi et al.
2015, Göker et al. 2009, Lutz & Piątek 2016). Due to previously allowed dual naming of several fungi, many uncertainties exist belonging the naming or treatment of several fungi (McNeill et al. 2012).
Because many smut species are very rare it is really important to use herbarium collections, to check morphology and of course if possible the phylogenetic features.
Some phylogenetic analysis within the smut fungi, also a small portion of that based on multigene analyses have shown, that many smut fungi still have an unclear position within the system (Begerow et al. 2006).
1.2.1 Taxonomic concepts in smut fungi
Smut fungi are biotrophic parasites that mostly produce black to brown masses of teliospores in different organs of plants. The teliospores germinate to form basidia and basidiospores that grow as a saprophytic haploid yeasts. These fungi were placed in the order Ustilaginales (Clinton 1906, Schröter 1889, Tulasne & Tulasne 1847, Zundel
1953). In this order, two families were described, the Ustilaginaceae and Tilletiaceae, based on the presence of phragmobasidia and holobasidia, respectively (Vánky 1987).
Vánky (2001) named teliospores-producing smuts as classical smut fungi and Begerow et al. (2006) proposed the name teliosporic smuts for these fungi. This classification system remained unchanged until Bauer et al. (1997) studied the septal pores and interaction zones between fungus and host cell. Bauer et al. (1997) recommended a new classification system for the smut fungi that challenged most of the accepted familial relationships. Begerow et al. (1997) supported this work based on genetic evaluations. Begerow et al. (1997) split the Ustilaginales into several lineages (see chapter 1.3.2). Based on these analyses the smut fungi were divided into two different classes, the teliosporic Ustilaginomycetes and the non-teliosporic Exobasidiomycetes, both belonging to the Ustilaginomycotina (Bauer et al. 2006).
Recently two further classes, the Malasseziomycetes and Monilliomycetes were included in the smut fungi (Wang et al. 2014).
Furthermore, these studies excluded some smut fungi from the Ustilaginomycotina.
For example, the Microbotryales, which mostly occur in the anthers of host species in the Caryophyllaceae, were found more closely related to rust fungi (Pucciniales) than to the Ustilaginomycotina (Bauer et al. 1997, Begerow et al. 1997). Some non-basidiomycetes fungi appear similar to smut fungi. For example, the genus Schroeteria G. Winter that occurs in the seeds of some host plants in Veronica L.
(Scrophulariaceae) produce black to dark blue spore masses (Vánky 1981) but belongs to the Ascomycota (Nagler 1989). Another example are the Protomycetaceae that produce yellow to white thickened spots (Reddy & Kramer 1975) that resemble smut fungi in the non-teliosporic genus Entyloma de Bary. Two further genera, Entorrhiza C.A. Weber and Talbotiomyces Vánky, R. Bauer & Begerow, were excluded from the Ustilaginomycotina, and transferred to a new phylum Entorrhizomycota (Bauer et al. 2015, Riess et al. 2015).
There are currently about 115 different genera with about 1.700 different species of Ustilaginomycotina that occur worldwide (Begerow et al. 2014). Vánky (2012) noted that one third of all smut fungi had only been found once, which demonstrates the rarity of many species. Most species of smut fungi infect only a few susceptible host species or often only one host plant species. Begerow et al. (2004a) evaluated the host lists from the European smut monograph (Vánky 1994) and found that only elven of 600 smut species had more than 20 hosts. The narrow host ranges of smut fungi
have been supported by phylogenetic analyses (e. g. Kruse et al. 2017 b, 2018 a,b, Li et al. 2017 a,b, Piątek et al. 2013, Stoll et al. 2003).
Most of the members of the Ustilaginomycotina, apart from some asexual taxa (see chapter 1.2.3) are plant parasites, especially on Poaceae (45%) and Cyperaceae (13%) (Begerow et al. 2014). Only a few species are associated with other tracheophytes, for example, Melaniella R. Bauer, Vánky, Begerow & Oberw. on spike mosses (Selaginella P. Beauv.), Exoteliospora R. Bauer, Oberw. & Vánky and Violaceomyces S.A. Albu, M. Toome & M.C. Aime on ferns, and Uleiella J. Schröt. on conifers (Albu et al. 2015, Vánky 2012).
There are some well-known economically important genera of smut fungi, for example, Ustilago (Pers.) Roussel (Ustilago-Sporisorium-Macalpinomyces-complex, Li et al. 2017b, McTaggart et al. 2012, 2016), Urocystis Rabenh. ex A.A. Fisch. Waldh.
(Lotze-Engelhard 2010) and Tilletia Tul. & C. Tul. (Castlebury et al. 2005). Some of the most significant smuts that cause great economic losses on graminicolous crops are Ustilago hordei (Pers.) Lagerh. (covered smut of barley), U. nuda (C.N. Jensen) Rostr. (loose smut of barley), U. tritici (Pers.) Rostr. (loose smut of wheat), U. maydis (DC.) Corda (corn smut), Urocystis agropyri (Preuss) A.A. Fisch. Waldh. (flag smut of wheat), Sporisorium reilianum (J.G. Kühn) Langdon & Full. (sorghum head smut), Sporisorium scitamineum (Syd.) M. Piepenbr., M. Stoll & Oberw. (sugar cane smut), Tilletia indica Mitra (karnal bunt of wheat and triticale), T. caries (DC.) Tul. & C. Tul.
(common bunt of wheat), and T. controversa J.G. Kühn (dwarf bunt of wheat) (Carris et al. 2006, Fischer & Holton 1957, Knogge 1996, Murray & Brennan 2009, 2010, Wilcoxson & Saari 1996).
1.2.2 Life cycle
Smut fungi are characterized by a dimorphic life cycle, i.e. a saprobic haploid yeast phase followed by a parasitic dicaryotic teliospore phase (de Bary 1884). The saprobic phase allows the smut fungus to survive away from their host as free living asexual anamorphic yeast that can be cultured. A hyphal growth within this phase has been observed for some Ustilaginomycotina (Begerow et al. 2014). Saprobic states of smut fungi occur on plants (Begerow et al. 2000, Sampaio 2004) but also on other substrates, e.g. soil, blood (Boekhout 2011, see chapter 1.2.3). The saprobic state ends with the conjugation of compatible haploid cells (plasmogamy). The parasitic
teliospore phase starts with mating (Kämper et al. 2006, Kellner et al. 2011) that precedes infection of the host plant, which is followed by intercellular mycelial growth.
Haustoria are produced in host cells that provide nutrition for the fungus. The formation of sori and production of teliospores concludes this parasitic phase. Some smut fungi have modified life cycles, e.g. do not produce teliospores (e.g. Exobasidiales, Microstromatales and Ceraceosorales) or do not have a diploid phase, which is typical for some yeasts (e. g. Malassezia).
1.2.3 Asexual smut fungi (Yeasts)
Besides the sexual smut fungi there is also an increasing knowledge since the beginning of the 21st century regarding lipophilic yeasts, occurring on endotherm species or various marine substrates or habitats. The genus Malassezia Baill., also belonging to the asexual yeasts, is the only one which is able to infect humans (Amend 2014, Ashbee 2007, Begerow et al. 2000, Boekhout et al. 2010, Cabañes 2014; Wang et al. 2014). Saprophytic ustilaginomycetous yeasts belong to many different genera and have been isolated from many ecosystems as well as from healthy plants (Albu et al. 2015, Amin et al. 2010, Begerow et al. 2000, Nasr et al. 2014, Padhi & Tayung 2013, Piątek et al. 2016, 2017, Rush & Aime 2013, Takahashi et al. 2011, Tanaka &
Honda 2017, Wang et al. 2014). These yeasts are not restricted to the smut fungi.
Worldwide there occur several different genera of asexual free living yeast in different habitats spreading over different fungal groups (Albu 2012, Aime et al. 2014, Avis et al. 2001, Boekhout 1995, Branda et al. 2010, Gai et al. 2009, Golubev & Sampaio 2009, Golubev et al. 2007, Inacio et al. 2002, Nakase 2000, Piątek et al. 2017, Rodriguez et al. 2008, Toome et al. 2013).
Wang et al. (2015) linked many different asexual ustilaginomycetous yeasts to teleomorphic stages. Currently, yeasts and yeast-like organisms belonging to the smut fungi (Ustilaginomycotina) are known from eleven different orders, namely, Entylomatales, Exobasidiales, Georgefischeriales, Golubeviales, Malasseziales, Microstromatales, Moniliellales, Robbauerales, Urocystidales, Ustilaginales, Violaceomycetales (Albu et al. 2015, Begerow et al. 2000; Boekhout et al. 2011, Nasr et al. 2014, Piątek et al. 2017, Rush & Aime 2013, Sampaio 2004, Tanaka & Honda 2017, Wang et al. 2014, 2015). Kruse et al. (2017b) and Wang et al. (2015) noted that some asexual smut yeasts were closely related to known sexual stages of smut fungi.
The distribution of asexual yeasts is strongly correlated with abiotic factors, especially the availability of metabolites (Fonseca & Inácio 2006).