Symptomatic plant viroid infections in phytopathogenic fungi

Shuang Wei, Ruiling Bian, Ida Bagus Andika, Erbo Niu, Qian Liu, Hideki Kondo, Liu Yang, Hongsheng Zhou, Tianxing Pang, Ziqian Lian, Xili Liu, Yunfeng Wu, Liying Sun

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)13042-13050
Number of pages9
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number26
DOIs
Publication statusPublished - 2019

Keywords

  • Fungus
  • Pathogenicity
  • Plant viroid |
  • Transmission

ASJC Scopus subject areas

  • General

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  • Cite this

    Wei, S., Bian, R., Andika, I. B., Niu, E., Liu, Q., Kondo, H., Yang, L., Zhou, H., Pang, T., Lian, Z., Liu, X., Wu, Y., & Sun, L. (2019). Symptomatic plant viroid infections in phytopathogenic fungi. Proceedings of the National Academy of Sciences of the United States of America, 116(26), 13042-13050. https://doi.org/10.1073/pnas.1900762116