Determinants of Coinfection in the Mycoviruses.

Coinfections of mycoviruses are generally common. The coinfecting mycoviruses are not necessarily the result of horizontal virus transmission among homologous fungal hosts compatible for anastomosis, but involve mycoviruses from phylogenetically diverse sources (Herrero and Zabalgogeazcoa, 2011; Osaki et al., 2016; Ran et al., 2016; Hao et al., 2018). An experimental study with different combinations of transmission scenarios among four partitiviruses showed a significant positive influence of one virus (Heterobasidion partitivirus13-an1) on its distantly related coinfecting partner Heterobasidion partitivirus 15-pa1, but no support of coinfection between two related viruses (Heterobasidion partitiviruses 11-au1 and 11-pa1) (Kashif et al., 2019). A more stable coinfection between distantly related species than conspecific strains was also reported among mycoviruses infecting the fungus, Heterobasidion parviporum (Vainio et al., 2015). Studies covering large geographical areas indicate that the mycoviruses in coinfections belong to the local fungal community (Ran et al., 2016; Arjona-Lopez et al., 2018). Arjona-Lopez et al. (2018) found a non-overlapping set of coinfecting mycoviruses in isolates of Rosellinia necatrix from Japan and the Mediterranean that match with mycoviruses from the respective local fungal pools. In general, transmission of mycoviruses occurs through anastomosis of vegetatively compatible strains of the same species, but phylogenetic evidence implies occasional transmission across vegetatively incompatible strains. The transmissions across vegetatively incompatible fungal hosts are poorly studied except in a few cases (Liu et al., 2003, 2016; Yaegashi et al., 2013a). In addition to transmission across heterologous fungi, interactions among mycoviruses play direct roles in coinfection. The interactions among coinfecting mycoviruses are diverse, ranging from synergistic to neutral to antagonistic. In some cases, mycovirus coinfection induces genome rearrangement of one of the coinfecting partners, likely through recombination (Sun and Suzuki, 2008). A more comprehensive review on the interactions among coinfecting mycoviruses is found in Hillman et al. (2018). The diversity of coinfecting mycoviruses and the diverse nature of interactions may imply that coinfections occur freely without any constraints. However, in examples from in vitro experiments the frequency of coinfection varies with different fungal systems and in many cases is lower than what would be expected from random incidences. For example, in 43 isolates of the ascomycete Tolypocladium cylindrosporum, coinfections of mycoviruses were reported in only in about 5% of the population (Herrero and Zabalgogeazcoa, 2011). In contrast, in almost 200 isolates of Ustilaginoidea virens examined multiple dsRNA elements were found in large samples, and the coinfection frequency of two common mycoviruses: Ustilaginoidea virens RNA virus 1 (Totiviridae) and Ustilaginoidea virens RNA virus 4 (unclassified) was close to 30% (Jiang et al., 2015). In our own study of about 200 North American isolates of Pseudogymnoascus destructans a fungus causing a deadly disease in bats, the coinfection incidence of a partitivirus (Thapa et al., 2016) and an unclassified mycovirus is close to 25%, but only in a geographically restricted area (unpublished). Independent segregation of coinfecting mycoviruses in the population has been described only in a few cases where the interaction is likely neutral, while in other cases one of the partners influences the presence of other. In the coinfection of two unrelated RNA viruses, Yado-nushi virus 1 (YnV1) and Yado-kari virus 1 (YkV1) in Rosellinia necatrix, YkV1 is dependent on YnV1. YkV1 does not segregate independently in the population (Zhang et al., 2016). Thus, the coinfection scenarios are likely influenced by the interactions between coinfecting viruses or at the level of mycovirus transmission, particularly during the transmission across vegetatively incompatible fungi or from other factors. Such constraints led us to investigate the determinants of mycovirus coinfections. Here, we discuss some of the determinants for mycovirus coinfection based on the literature available and provide our opinions on coinfection biology.