Proceedings of the National Academy of Sciences | 2019

Symptomatic plant viroid infections in phytopathogenic fungi



Significance Viroids are the only known autonomously replicating pathogenic agents that do not encode proteins. As viroids are known only to naturally infect plants, their infectivity and pathogenicity in other eukaryotes are largely unexplored. Herein, we demonstrate the stable infection of three viroid species in different plant pathogenic filamentous fungi and show that viroid infection can reduce the growth and virulence of fungi. In addition to successful viroid RNA inoculation of fungal spheroplasts, viroid infection of fungus could occur through viroid transmission from the plant and when viroid RNAs are directly applied to fungal mycelia. These findings are relevant to our understanding of viroid replication, transmission, and pathogenicity. Viroids are pathogenic agents that have a small, circular noncoding RNA genome. They have been found only in plant species; therefore, their infectivity and pathogenicity in other organisms remain largely unexplored. In this study, we investigate whether plant viroids can replicate and induce symptoms in filamentous fungi. Seven plant viroids representing viroid groups that replicate in either the nucleus or chloroplast of plant cells were inoculated to three plant pathogenic fungi, Cryphonectria parasitica, Valsa mali, and Fusarium graminearum. By transfection of fungal spheroplasts with viroid RNA transcripts, each of the three, hop stunt viroid (HSVd), iresine 1 viroid, and avocado sunblotch viroid, can stably replicate in at least one of those fungi. The viroids are horizontally transmitted through hyphal anastomosis and vertically through conidia. HSVd infection severely debilitates the growth of V. mali but not that of the other two fungi, while in F. graminearum and C. parasitica, with deletion of dicer-like genes, the primary components of the RNA-silencing pathway, HSVd accumulation increases. We further demonstrate that HSVd can be bidirectionally transferred between F. graminearum and plants during infection. The viroids also efficiently infect fungi and induce disease symptoms when the viroid RNAs are exogenously applied to the fungal mycelia. These findings enhance our understanding of viroid replication, host range, and pathogenicity, and of their potential spread to other organisms in nature.

Volume 116
Pages 13042 - 13050
DOI 10.1073/pnas.1900762116
Language English
Journal Proceedings of the National Academy of Sciences

Full Text