Skip to main content

Advertisement

SpringerLink
Log in

A novel double-stranded RNA mycovirus from Fusarium graminearum: nucleic acid sequence and genomic structure

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Ten Fusarium graminearum isolates from China were screened for dsRNA mycoviruses. Five dsRNAs (2.4 to 3.5 kbp) were purified from isolate China 9, cloned, and sequenced. BLAST analysis showed that the proteins encoded by dsRNA1 possess motifs that are conserved in RNA-dependent RNA polymerases, dsRNA2 resembles the hypothetical protein encoded by dsRNA3 of Magnaporthe oryzae chrysovirus 1, dsRNA4 shares no significant similarity to any published protein, and dsRNA5 has a C2H2 zinc finger domain. Tandem mass spectrophotometry, surface protein labeling of virus-like particles, SDS-PAGE, and protein BLAST results supports the notion that three of the virus segments code for structural proteins, of which dsRNA3 possibly codes for the capsid protein. Relative quantitative RT-PCR studies of the 5 dsRNAs suggested that the segments are encapsidated separately in unequal amounts. Genomic structure and phylogenic studies support the possibility that this virus may be a candidate for the type species of a novel genus in the family Chrysoviridae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Ahlquist P (1999) Bromoviruses (Bromoviridae) p. 198–204. In: Granoff A, Webster RG (eds) Encyclopedia of Virology, 2nd edn. Academic Press, San Diego

    Google Scholar 

  2. Aoki N, Moriyama H, Kodama M, Arie T, Teraoka T, Fukuhara T (2009) A novel mycovirus associated with four double-stranded RNAs affects host fungal growth in Alternaria alternata. Virus Res 140:179–187

    Article  PubMed  CAS  Google Scholar 

  3. Attoui H, De Micco P, de Lamballerie X (1997) Complete nucleotide sequence of Colorado tick fever virus segments M6, S1 and S2. J Gen Virol 78(Pt 11):2895–2899

    PubMed  CAS  Google Scholar 

  4. Boukhvalova MS, Prince GA, Blanco JC (2010) Inactivation of respiratory syncytial virus by zinc finger reactive compounds. Virol J 7:20

    Article  PubMed  Google Scholar 

  5. Bruenn JA (1993) A closely related group of RNA-dependent RNA polymerases from double-stranded RNA viruses. Nucleic Acids Res 21:5667–5669

    Article  PubMed  CAS  Google Scholar 

  6. Castro M, Kramer K, Valdivia L, Ortiz S, Castillo A (2003) A double-stranded RNA mycovirus confers hypovirulence-associated traits to Botrytis cinerea. FEMS Microbiol Lett 228:87–91

    Article  PubMed  CAS  Google Scholar 

  7. Chiba S, Salaipeth L, Lin YH, Sasaki A, Kanematsu S, Suzuki N (2009) A novel bipartite double-stranded RNA nycovirus from the white root rot fungus Rosellinia necatrix: molecular and biological characterization, taxonomic considerations, and potential for biological control. J Virol 83:12801–12812

    Article  PubMed  CAS  Google Scholar 

  8. Chu YM, Jeon JJ, Yea SJ, Kim YH, Yun SH, Lee YW, Kim KH (2002) Double-stranded RNA mycovirus from Fusarium graminearum. Appl Environ Microbiol 68:2529–2534

    Article  PubMed  CAS  Google Scholar 

  9. Chu YM, Lim WS, Yea SJ, Cho JD, Lee YW, Kim KH (2004) Complexity of dsRNA mycovirus isolated from Fusarium graminearum. Virus Genes 28:135–143

    Article  PubMed  CAS  Google Scholar 

  10. Darissa O, Willingmann P, Adam G (2010) Optimized approaches for the sequence determination of double-stranded RNA templates. J Virol Methods 169:397–403

    Article  PubMed  CAS  Google Scholar 

  11. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  12. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (2005) Virus Taxonomy, VIIIth Report of the ICTV. Elsevier/Academic Press, London

    Google Scholar 

  13. Finerty PJ Jr, Bass BL (1997) A Xenopus zinc finger protein that specifically binds dsRNA and RNA-DNA hybrids. J Mol Biol 271:195–208

    Article  PubMed  CAS  Google Scholar 

  14. Gallie DR, Walbot V (1992) Identification of the motifs within the tobacco mosaic virus 5’-leader responsible for enhancing translation. Nucleic Acids Res 20:4631–4638

    Article  PubMed  CAS  Google Scholar 

  15. Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384

    Article  PubMed  CAS  Google Scholar 

  16. Hammond TM, Andrewski MD, Roossinck MJ, Keller NP (2008) Aspergillus mycoviruses are targets and suppressors of RNA silencing. Eukaryot Cell 7:350–357

    Article  PubMed  CAS  Google Scholar 

  17. Iuchi S (2001) Three classes of C2H2 zinc finger proteins. Cell Mol Life Sci 58:625–635

    Article  PubMed  CAS  Google Scholar 

  18. Jiang D, Ghabrial SA (2004) Molecular characterization of Penicillium chrysogenum virus: reconsideration of the taxonomy of the genus Chrysovirus. J Gen Virol 85:2111–2121

    Article  PubMed  CAS  Google Scholar 

  19. Kuang M, Goodin MM, Schlagnhaufer C, Schlagnhaufer B, Romaine CP (2004) Molecular genetic analysis of double-stranded RNA viruses in Agaricus bisporus. Mush. Sci 16:507–513

    CAS  Google Scholar 

  20. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  21. Leach J, Lang BR, Yoder OC (1982) Methods for selection of mutants and in vitro culture of Cochliobolus heterostrophus. J Gen Microbiol 128:1719–1729

    Google Scholar 

  22. McCabe PM, Pfeiffer P, Van Alfen NK (1999) The influence of dsRNA viruses on the biology of plant pathogenic fungi. Trends Microbiol 7:377–381

    Article  PubMed  CAS  Google Scholar 

  23. Mertens PP, Sangar DV (1985) Analysis of the terminal sequences of the genome segments of four orbiviruses. Prog Clin Biol Res 178:371–387

    PubMed  CAS  Google Scholar 

  24. Ninet B, Jan I, Bontems O, Lechenne B, Jousson O, Lew D, Schrenzel J, Panizzon RG, Monod M (2005) Molecular identification of Fusarium species in onychomycoses. Dermatology 210:21–25

    Article  PubMed  Google Scholar 

  25. Nuss DL (2005) Hypovirulence: mycoviruses at the fungal-plant interface. Nat Rev Microbiol 3:632–642

    Article  PubMed  CAS  Google Scholar 

  26. Pearson MN, Beever RE, Boine B, Arthur K (2009) Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol 10:115–128

    Article  PubMed  CAS  Google Scholar 

  27. Persikov AV, Osada R, Singh M (2009) Predicting DNA recognition by Cys2His2 zinc finger proteins. Bioinformatics 25:22–29

    Article  PubMed  CAS  Google Scholar 

  28. Preisig O, Moleleki N, Smit WA, Wingfield BD, Wingfield MJ (2000) A novel RNA mycovirus in a hypovirulent isolate of the plant pathogen Diaporthe ambigua. J Gen Virol 81:3107–3114

    PubMed  CAS  Google Scholar 

  29. Romaine CP, Schlagnhaufer B (1995) PCR analysis of the viral complex associated with La France disease of Agaricus bisporus. Appl Environ Microbiol 61:2322–2325

    PubMed  CAS  Google Scholar 

  30. Soldevila AI, Havens WH, Ghabrial SA (2000) A cellular protein with an RNA-binding activity co-purifies with viral dsRNA form mycovirus-infected Helminthosporium victoriae. Virology 20:183–190

    Article  Google Scholar 

  31. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  32. Tanchou V, Decimo D, Pechoux C, Lener D, Rogemond V, Berthoux L, Ottmann M, Darlix JL (1998) Role of the N-terminal zinc finger of human immunodeficiency virus type 1 nucleocapsid protein in virus structure and replication. J Virol 72:4442–4447

    PubMed  CAS  Google Scholar 

  33. Theisen S, Roeseler S, Berger S, Buchenauer H (2001) Analysis of double-stranded RNA and virus-like particles in trichothecene-producing strains of Fusarium graminearum. Mycotoxin Res 17:32–36

    Article  Google Scholar 

  34. Tsai RY, Reed RR (1998) Identification of DNA recognition sequences and protein interaction domains of the multiple-Zn-finger protein Roaz. Mol Cell Biol 18:6447–6456

    PubMed  CAS  Google Scholar 

  35. Urayama S, Kato S, Suzuki Y, Aoki N, Le MT, Arie T, Teraoka T, Fukuhara T, Moriyama H (2010) Mycoviruses related to chrysovirus affect vegetative growth in the rice blast fungus Magnaporthe oryzae. J Gen Virol (2010), In Press, doi 10.1099/vir.0.025411-0

  36. van Diepeningen AD, Debets AJ, Hoekstra RF (2006) Dynamics of dsRNA mycoviruses in black Aspergillus populations. Fungal Genet Biol 43:446–452

    Article  PubMed  Google Scholar 

  37. van Diepeningen AD, Debets AJ, Hoekstra RF (1998) Intra- and interspecies virus transfer in Aspergilli via protoplast fusion. Fungal Genet Biol 25:171–180

    Article  PubMed  Google Scholar 

  38. Xie J, Wei D, Jiang D, Fu Y, Li G, Ghabrial S, Peng Y (2006) Characterization of debilitation-associated mycovirus infecting the plant-pathogenic fungus Sclerotinia sclerotiorum. J Gen Virol 87:241–249

    Article  PubMed  CAS  Google Scholar 

  39. Yu J, Kwon SJ, Lee KM, Son M, Kim KH (2009) Complete nucleotide sequence of double-stranded RNA viruses from Fusarium graminearum strain DK3. Arch Virol 154:1855–1858

    Article  PubMed  CAS  Google Scholar 

  40. 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 U S A 107:8387–8392

    Article  PubMed  CAS  Google Scholar 

  41. Zhang L, Fu Y, Xie J, Jiang D, Li G, Yi X (2009) A novel virus that infecting hypovirulent strain XG36–1 of plant fungal pathogen Sclerotinia sclerotiorum. Virol J 6:96

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

We thank J. Mehrmann for assistance with electron microscopy, F. Buck for the help with protein sequencing, and C. Voigt for access to his real-time PCR machine. OD was supported by the Deutsche Akademische Austausch Dienst (DAAD).

Author information

Authors and Affiliations

  1. Fachbereich Biologie, Biozentrum Klein Flottbeck, Universität Hamburg, Ohnhorststr. 18, 22609, Hamburg, Germany

    Omar Darissa, Peter Willingmann, Wilhelm Schäfer & Günter Adam

Authors
  1. Omar Darissa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Willingmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wilhelm Schäfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Günter Adam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Omar Darissa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Darissa, O., Willingmann, P., Schäfer, W. et al. A novel double-stranded RNA mycovirus from Fusarium graminearum: nucleic acid sequence and genomic structure. Arch Virol 156, 647–658 (2011). https://doi.org/10.1007/s00705-010-0904-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-010-0904-9

Keywords

Search

Navigation