Molecular characterization of a novel mycovirus in Alternaria alternata manifesting two-sided effects: Down-regulation of host growth and up-regulation of host plant pathogenicity

Highlights: • A novel mycovirus exhibiting two contrasting effects, attenuating and hypervirulent. • High-titer mycovirus causes a severe impaired growth phenotype in host fungus. • Mycoviral protein is highly expressed in isolates with high dsRNA titer. • Expression of mycoviral protein in S. cerevisiae induces cytological damage. • High-titer mycovirus confers host fungus with hypervirulence in a plant infection. A double-stranded RNA (dsRNA) mycovirus was detected in a strain of Alternaria alternata showing impaired growth phenotypes. The A. alternata strain is the Japanese pear pathotype, which produces a host-specific AK-toxin. Sequence analysis of the viral genome dsRNAs revealed that this mycovirus consists of five dsRNAs and is evolutionarily related to members of the family Chrysoviridae; the virus was named Alternaria alternata chrysovirus 1 (AaCV1). AaCV1-ORF2 protein accumulated in dsRNA-high-titer sub-isolates with severely impaired phenotypes; heterologous AaCV1-ORF2 overexpression in Saccharomyces cerevisiae caused growth inhibition. In contrast to this yeast growth inhibition phenomenon, the dsRNA-high-titer isolates displayed enhanced pathogenicity against Japanese pear plants, in accordance with a 13-fold increase in AK-toxin level in one such isolate. These findings indicated that AaCV1 is a novel mycovirus that exhibits two contrasting effects, impairing growth of the host fungus while rendering the host 'hypervirulent' to the plant.