A rapidly growing number of viruses of lower eukaryotes have been reported in the past few decades. These have enhanced our understanding of virus evolution and diversity. Simultaneously, some unusual viruses have challenged or broken the “common rules” of viruses in sizes and concepts. One such virus group includes the so called dsDNA megaviruses isolated from amoebae that exceed some bacterial parasites in coding capacity and particle size. Other unusual viruses have been found in fungi that include “naked” or “capsidless” RNA viruses unable to form virus particles, exemplified by hypoviruses and narnaviruses. Also among them are fungal multi-segmented dsRNA viruses that are infectious viruses as naked dsRNA. My laboratory also had an opportunity to discover such a virus from an important plant pathogenic fungus, Rosellinia necatrix. The fungus is a filamentous ascomycete that causes white root rot in diverse perennial crops. A mixed viral infection was found in a hypovirulent strain of R. necatrix. Co-infecting viruses were termed Yado-kari virus 1 (YkV1) with a positive strand (+) RNA genome of approximately 6 kb and Yado-nushi virus 1 (YnV1) with a double-stranded (ds) RNA genome of approximately 9 kb. “Yado” in Japanese literally means home or house, while “kari” and “nushi” refer to “borrower” and “owner,” respectively. Herewith, we show unique mutualistic interactions representing a new virus lifestyle: a capsidless (+) RNA virus, YkV1, hosted by a dsRNA virus YnV1. According to our proposed model (Zhang et al., Nat Microbiol, 2016), YnV1 is an independent virus able to complete its replication cycle like other dsRNA viruses, while YkV1 diverts YnV1 CP as the replication sites where trans-encased YkV1 RdRp synthesizes its own RNA as if it were a dsRNA virus. Furthermore, YkV1 was shown to enhance YnV1 accumulation. Some data with site-directed mutagenesis of available infectious YkV1 cDNA supported the model. This model still needs to be further validated by biochemical analysis with purified heterocapsids. There may be similar mutualistic interactions in other fungi such as Aspergillus foetidus (Kozlakidis et al., 2013; Nerva et al., 2016; Osaki et al., 2016). We propose the family Yadokariviridae that accommodates YkV1 and these related viruses. Their evolutionary implication and comparisons with subviral molecules similar to YkV1 will be discussed in this presentation.
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