Advertisement

Characterization of a novel victorivirus isolated from the phytopathogenic fungus Botryosphaeria dothidea

  • Mengmeng Yang
  • Lifeng Zhai
  • Feng Xiao
  • Yashuang Guo
  • Min Fu
  • Ni Hong
  • Guoping WangEmail author
Original Article
  • 40 Downloads

Abstract

Botryosphaeria dothidea is an important pathogenic fungus that causes serious diseases in fruits and trunks of many wood plant species worldwide. In this study, 28 B. dothidea strains isolated from pear trunk samples showing stem wart or canker symptoms were used to detect double-stranded RNA (dsRNA) viruses. The dsRNA bands with the size of ~ 1.0 to ~ 6.0 kbp were examined from ten strains. Here, we reported a novel dsRNA mycovirus, tentatively named as Botryosphaeria dothidea victorivirus 2 (BdVV2), isolated from the B. dothidea strain MSD53. BdVV2 contained spherical virions that were ~ 38 nm in diameter consisting of a single linear dsRNA genome of 5,090 bp in length. The BdVV2 genome contained two overlapping open reading frames (ORFs) encoding a putative coat protein (CP) and an RNA-dependent RNA polymerase (RdRp), which shared significant amino acid identities of 68% and 60% with the corresponding proteins of Sphaeropsis sapinea RNA viruses 1 (SsRV1). Phylogenetic analyses based on the aa sequences of CP and RdRp both showed that BdVV2 was phylogenetically related to the members of the genus Victorivirus in the family Totiviridae. BdVV2 is thus a novel victorivirus isolated from the phytopathogenic fungus B. dothidea.

Notes

Acknowledgements

This work was financially supported by the earmarked fund for Pear Modern Agro-Industry Technology Research System (CARS-28-15) of the Chinese Ministry of Agriculture and the Fundamental Research Funds for the Central Universities (no. 2662016PY107).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

No human or animal ethics approval was required for the completion of this study.

Informed consent

Informed consent was obtained from all individual participants included in this study.

References

  1. 1.
    Bruenn JA (2003) A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases. Nucleic Acids Res 31:1821–1829CrossRefGoogle Scholar
  2. 2.
    Burland TG (2000) DNASTAR’s Lasergene sequence analysis software. Methods Mol Biol 132:71–91Google Scholar
  3. 3.
    Chiba S, Suzuki N (2015) Highly activated RNA silencing via strong induction of dicer by one virus can interfere with the replication of an unrelated virus. Proc Natl Acad Sci USA 112:E4911–E4918CrossRefGoogle Scholar
  4. 4.
    Choi GH, Nuss DL (1992) Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science 257:800–803CrossRefGoogle Scholar
  5. 5.
    Ding Z, Zhou T, Guo LY (2017) Characterization of a novel strain of Botryosphaeria dothidea chrysovirus 1 from the apple white rot pathogen Botryosphaeria dothidea. Arch Virol 162:2097–2102CrossRefGoogle Scholar
  6. 6.
    Donaire L, Pagan I, Ayllon MA (2016) Characterization of Botrytis cinerea negative-stranded RNA virus 1, a new mycovirus related to plant viruses, and a reconstruction of host pattern evolution in negative-sense ssRNA viruses. Virology 499:212–218CrossRefGoogle Scholar
  7. 7.
    Ghabrial SA, Nibert ML (2009) Victorivirus, a new genus of fungal viruses in the family Totiviridae. Arch Virol 154:373–379CrossRefGoogle Scholar
  8. 8.
    Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384CrossRefGoogle Scholar
  9. 9.
    Ghabrial SA, Caston JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368CrossRefGoogle Scholar
  10. 10.
    Herrero N, Zabalgogeazcoa I (2011) Mycoviruses infecting the endophytic and entomopathogenic fungus Tolypocladium cylindrosporum. Virus Res 160:409–413CrossRefGoogle Scholar
  11. 11.
    Herrero N, Duenas E, Quesada-Moraga E, Zabalgogeazcoa I (2012) Prevalence and diversity of viruses in the entomopathogenic fungus Beauveria bassiana. Appl Environ Microbiol 78:8523–8530CrossRefGoogle Scholar
  12. 12.
    Herrero N (2016) A novel monopartite dsRNA virus isolated from the entomopathogenic and nematophagous fungus Purpureocillium lilacinum. Arch Virol 161:3375–3384CrossRefGoogle Scholar
  13. 13.
    Huang S, Soldevila AI, Webb BA, Ghabrial SA (1997) Expression, assembly, and proteolytic processing of Helminthosporium victoriae 190S totivirus capsid protein in insect cells. Virology 234:130–137CrossRefGoogle Scholar
  14. 14.
    Ikeda Y, Shimura H, Kitahara R, Masuta C, Ezawa T (2012) A novel virus-like double-stranded RNA in an obligate biotroph arbuscular mycorrhizal fungus: a hidden player in mycorrhizal symbiosis. Mol Plant Microbe Interact 25:1005–1012CrossRefGoogle Scholar
  15. 15.
    Kanhayuwa L, Kotta-Loizou I, Özkan S, Gunning AP, Coutts RHA (2015) A novel mycovirus from Aspergillus fumigatus contains four unique dsRNAs as its genome and is infectious as dsRNA. Proc Natl Acad Sci USA 112:9100–9105CrossRefGoogle Scholar
  16. 16.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  17. 17.
    Lin H, Lan X, Liao H, Parsley TB, Nuss DL, Chen B (2007) Genome sequence, full-length infectious cDNA clone, and mapping of viral double-stranded RNA accumulation determinant of hypovirus CHV1-EP721. J Virol 81:1813–1820CrossRefGoogle Scholar
  18. 18.
    Liu H, Fu Y, Jiang D, Li G, Xie J, Peng Y, Yi X, Ghabrial SA (2009) A novel mycovirus that is related to the human pathogen Hepatitis E virus and Rubi-like viruses. J Virol 83:1981–1991CrossRefGoogle Scholar
  19. 19.
    Liu L, Xie J, Cheng J, Fu Y, Li G, Yi X, Jiang D (2014) Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses. Proc Natl Acad Sci USA 111:12205–12210CrossRefGoogle Scholar
  20. 20.
    Pearson MN, Beever RE, Boine B, Arthur K (2009) Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol 10:115–128CrossRefGoogle Scholar
  21. 21.
    Phillips AJ, Rumbos IC, Alves A, Correia A (2005) Morphology and phylogeny of Botryosphaeria dothidea causing fruit rot of olives. Mycopathologia 159:433–439CrossRefGoogle Scholar
  22. 22.
    Preisig O, Wingfield BD, Wingfield MJ (1998) Coinfection of a fungal pathogen by two distinct double-stranded RNA viruses. Virology 252:399–406CrossRefGoogle Scholar
  23. 23.
    Soldevila AI, Ghabrial SA (2000) Expression of the totivirus Helminthosporium victoriae 190S virus RNA-dependent RNA polymerase from its downstream open reading frame in dicistronic constructs. J Virol 74:997–1003CrossRefGoogle Scholar
  24. 24.
    Turina M, Ghignone S, Astolfi N, Silvestri A, Bonfante P, Lanfranco L (2018) The virome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals the first report of DNA fragments corresponding to replicating non-retroviral RNA viruses in fungi. Environ Microbiol 20:2012–2025CrossRefGoogle Scholar
  25. 25.
    Vainio EJ, Muller MM, Korhonen K, Piri T, Hantula J (2015) Viruses accumulate in aging infection centers of a fungal forest pathogen. ISME J 9:497–507CrossRefGoogle Scholar
  26. 26.
    Wang L, Jiang J, Wang Y, Hong N, Zhang F, Xu W, Wang G (2014) Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus. J Virol 88:7517–7527CrossRefGoogle Scholar
  27. 27.
    Wu S, Cheng J, Fu Y, Chen T, Jiang D, Ghabrial SA, Xie J (2017) Virus-mediated suppression of host non-self recognition facilitates horizontal transmission of heterologous viruses. PLoS Pathog 13:e1006234CrossRefGoogle Scholar
  28. 28.
    Xiang J, Fu M, Hong N, Zhai L, Xiao F, Wang G (2017) Characterization of a novel botybirnavirus isolated from a phytopathogenic Alternaria fungus. Arch Virol 162:3907–3911CrossRefGoogle Scholar
  29. 29.
    Yaegashi H, Nakamura H, Sawahata T, Sasaki A, Iwanami Y, Ito T, Kanematsu S (2013) Appearance of mycovirus-like double-stranded RNAs in the white root rot fungus, Rosellinia necatrix, in an apple orchard. FEMS Microbiol Ecol 83:49–62CrossRefGoogle Scholar
  30. 30.
    Yaegashi H, Shimizu T, Ito T, Kanematsu S (2016) Differential inductions of RNA silencing among encapsidated double-stranded RNA mycoviruses in the white root rot fungus Rosellinia necatrix. J Virol 90:5677–5692CrossRefGoogle Scholar
  31. 31.
    Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107:8387–8392CrossRefGoogle Scholar
  32. 32.
    Zhai L, Zhang M, Lv G, Chen X, Jia N, Hong N, Wang G (2014) Biological and molecular characterization of four Botryosphaeria species isolated from pear plants showing stem wart and stem canker in China. Plant Dis 98:716–726CrossRefGoogle Scholar
  33. 33.
    Zhai L, Hong N, Zhang M, Wang G (2015) Complete dsRNA sequence of a novel victorivirus isolated from the pear stem wart fungus Botryosphaeria dothidea. Arch Virol 160:613–616CrossRefGoogle Scholar
  34. 34.
    Zhai L, Xiang J, Zhang M, Fu M, Yang Z, Hong N, Wang G (2016) Characterization of a novel double-stranded RNA mycovirus conferring hypovirulence from the phytopathogenic fungus Botryosphaeria dothidea. Virology 493:75–85CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Mengmeng Yang
    • 1
    • 2
    • 4
  • Lifeng Zhai
    • 3
  • Feng Xiao
    • 2
    • 4
  • Yashuang Guo
    • 2
    • 4
  • Min Fu
    • 2
    • 4
  • Ni Hong
    • 1
    • 2
    • 4
  • Guoping Wang
    • 1
    • 2
    • 4
    Email author
  1. 1.State Key Laboratory of Agricultural MicrobiologyHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  2. 2.College of Plant Science and TechnologyHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  3. 3.College of Life Science and TechnologyYangtze Normal UniversityChongqingPeople’s Republic of China
  4. 4.Key Lab of Plant Pathology of Hubei ProvinceWuhanPeople’s Republic of China

Personalised recommendations