Advertisement

Archives of Virology

, Volume 164, Issue 2, pp 567–572 | Cite as

Phytophthora infestans RNA virus 2, a novel RNA virus from Phytophthora infestans, does not belong to any known virus group

  • Guohong CaiEmail author
  • Kevin Myers
  • William E. Fry
  • Bradley I. HillmanEmail author
Brief Report

Abstract

Phytophthora infestans is the causal agent of potato and tomato late blight. In this study, we obtained the complete genome sequence of a novel RNA virus from this plant pathogen, tentatively named “Phytophthora infestans RNA virus 2” (PiRV-2). The PiRV-2 genome is 11,170 nt in length and lacks a polyA tail. It contains a single large open reading frame (ORF) with short 5’ and 3’ untranslated regions. The ORF is predicted to encode a polyprotein of 3710 aa (calculated molecular weight, 410.94 kDa). This virus lacks significant similarity to any other known viruses, even in the conserved RNA-dependent RNA polymerase region. Phylogenetic analysis demonstrated that it did not cluster with any known virus group. We conclude that PiRV-2 belongs to a new virus family yet to be described. This virus was found to be faithfully transmitted through asexual reproduction.

References

  1. 1.
    Attoui H, Billoir F, Cantaloube JF, Biagini P, de Micco P, de Lamballerie X (2000) Strategies for the sequence determination of viral dsRNA genomes. J Virol Methods 89:147–158CrossRefGoogle Scholar
  2. 2.
    Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977CrossRefGoogle Scholar
  3. 3.
    Buck KW (1986) Fungal virology-an overview. In: Buck KW (ed) Fungal virology. CRC Press Inc., Boca Raton, p 1084Google Scholar
  4. 4.
    Cai G, Myers K, Hillman BI, Fry WE (2009) A novel virus of the late blight pathogen, Phytophthora infestans, with two RNA segments and a supergroup 1 RNA-dependent RNA polymerase. Virology 392:52–61CrossRefGoogle Scholar
  5. 5.
    Cai G, Myers K, Fry WE, Hillman BI (2012) A member of the virus family Narnaviridae from the plant pathogenic oomycete Phytophthora infestans. Arch Virol 157:165–169CrossRefGoogle Scholar
  6. 6.
    Cai G, Hillman BI (2013) Phytophthora viruses. In: Said AG (ed) Adv virus res. Academic Press, Cambridge, pp 327–350Google Scholar
  7. 7.
    Cai G, Krychiw JF, Myers K, Fry WE, Hillman BI (2013) A new virus from the plant pathogenic oomycete Phytophthora infestans with an 8 kb dsRNA genome: the sixth member of a proposed new virus genus. Virology 435:341–349CrossRefGoogle Scholar
  8. 8.
    Cavalier-Smith T (2000) Membrane heredity and early chloroplast evolution. Trends Plant Sci 5:174–182CrossRefGoogle Scholar
  9. 9.
    Gahan PB (2005) dsRNA genetic elements, concepts and applications in agriculture, forestry and medicine. Cell Biochem Funct 23:147CrossRefGoogle Scholar
  10. 10.
    Gillings MR, Tesoriero LA, Gunn LV (1993) Detection of double-stranded RNA and virus-like particles in Australian isolates of Pythium irregulare. Plant Pathol 42:6–15CrossRefGoogle Scholar
  11. 11.
    Gulya TJ (1992) Ultrastructure of virus-like particles in Plasmopara halstedii. Can J Bot 70:334–339CrossRefGoogle Scholar
  12. 12.
    Hacker CV, Brasier CM, Buck KW (2005) A double-stranded RNA from a Phytophthora species is related to the plant endornaviruses and contains a putative UDP glycosyltransferase gene. J Gen Virol 86:1561–1570CrossRefGoogle Scholar
  13. 13.
    Hansen JL, Long AM, Schultz SC (1997) Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5:1109–1122CrossRefGoogle Scholar
  14. 14.
    Heller-Dohmen M, Göpfert JC, Hammerschimdt R, Spring O (2008) Different pathotypes of the sunflower downy mildew pathogen Plasmopara halstedii all contain isometric virions. Mol Plant Pathol 9:777–786CrossRefGoogle Scholar
  15. 15.
    Heller-Dohmen M, Göpfert JC, Pfannstiel J, Spring O (2011) The nucleotide sequence and genome organization of Plasmopara halstedii virus. Virol J 8:123CrossRefGoogle Scholar
  16. 16.
    Hofmann K, Butcher P, Falquet L, Bairoch A (1999) The PROSITE database, its status in 1999. Nucleic Acids Res 27:215–219CrossRefGoogle Scholar
  17. 17.
    Honkura R, Shirako Y, Ehara Y, Yamanaka S (1983) Two types of virus-like particles isolated from downy mildew diseased rice plants. Jpn J Phytopathol 49:653–658CrossRefGoogle Scholar
  18. 18.
    Hulo N, Bairoch A, Bulliard V, Cerutti L, De Castro E, Langendijk-Genevaux PS, Pagni M, Sigrist CJA (2006) The PROSITE database. Nucl Acids Res 34:D227–D230CrossRefGoogle Scholar
  19. 19.
    Judelson HS, Fabritius AL (2000) A linear RNA replicon from the oomycete Phytophthora infestans. Mol Gen Genet 263:395–403CrossRefGoogle Scholar
  20. 20.
    Klassen GR, Kim WK, Barr DJS, Desaulniers NL (1991) Presence of double-stranded RNA in isolates of Pythium irregulare. Mycologia 83:657–661CrossRefGoogle Scholar
  21. 21.
    Koonin EV, Dolja VV, Morris TJ (1993) Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28:375–430CrossRefGoogle Scholar
  22. 22.
    Kozak M (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283–292CrossRefGoogle Scholar
  23. 23.
    Kozak M (1987) An analysis of 5’-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 15:8125–8148CrossRefGoogle Scholar
  24. 24.
    Kozlakidis Z, Brown NA, Jamal A, Phoon X, Coutts RHA (2009) Incidence of endornaviruses in Phytophthora taxon douglasfir and Phytophthora ramorum. Virus Genes 40:130CrossRefGoogle Scholar
  25. 25.
    Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes1. J Mol Biol 305:567–580CrossRefGoogle Scholar
  26. 26.
    Lambden PR, Cooke SJ, Caul EO, Clarke IN (1992) Cloning of noncultivatable human rotavirus by single primer amplification. J Virol 66:1817–1822Google Scholar
  27. 27.
    Lutcke HA, Chow KC, Mickel FS, Moss KA, Kern HF, Scheele GA (1987) Selection of AUG initiation codons differs in plants and animals. EMBO J 6:43–48CrossRefGoogle Scholar
  28. 28.
    Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331CrossRefGoogle Scholar
  29. 29.
    Morris TJ, Dodds JA (1979) Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858CrossRefGoogle Scholar
  30. 30.
    Newhouse JR, Tooley PW, Smith OP, Fishel RA (1992) Characterization of double-stranded RNA in isolates of Phytophthora infestans from Mexico, the Netherlands, and Peru. Phytopathology 82:164–169CrossRefGoogle Scholar
  31. 31.
    Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Meth 8:785–786CrossRefGoogle Scholar
  32. 32.
    Roos UP, Shaw DS (1985) Intranuclear virus-like particles in a laboratory strain of Phytophthora drechsleri. Trans Br Mycol Soc 84:340–344CrossRefGoogle Scholar
  33. 33.
    Sasai S, Tamura K, Tojo M, Herrero M-L, Hoshino T, Ohki ST, Mochizuki T (2018) A novel non-segmented double-stranded RNA virus from an Arctic isolate of Pythium polare. Virology 522:234–243CrossRefGoogle Scholar
  34. 34.
    Shirako Y, Ehara Y (1985) Composition of viruses isolated from Sclerophthora macrospora-infected rice plants. Jpn J Phytopathol 51:459–464CrossRefGoogle Scholar
  35. 35.
    Shwed PS, Dobos P, Cameron LA, Vakharia VN, Duncan R (2002) Birnavirus VP1 proteins form a distinct subgroup of RNA-dependent RNA polymerases lacking a GDD motif. Virology 296:241–250CrossRefGoogle Scholar
  36. 36.
    Sogin ML, Silberman JD (1998) Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int J Parasitol 28:11–20CrossRefGoogle Scholar
  37. 37.
    Styer EL, Corbett MK (1978) Intranuclear virus-like particles of Phytophthora infestans and P. parasitica var. parasitica. Mycovirus Newsl 6:16–18Google Scholar
  38. 38.
    Suzuki N, Sugawara M, Kusano T, Mori H, Matsuura Y (1994) Immunodetection of rice dwarf phytoreoviral proteins in both insect and plant hosts. Virology 202:41–48CrossRefGoogle Scholar
  39. 39.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  40. 40.
    Tooley PW, Hewings AD, Falkenstein KF (1989) Detection of double-stranded RNA in Phytophthora infestans. Phytopathology 79:470–474CrossRefGoogle Scholar
  41. 41.
    Yokoi T, Takemoto Y, Suzuki M, Yamashita S, Hibi T (1999) The nucleotide sequence and genome organization of Sclerophthora macrospora virus B. Virology 264:344–349CrossRefGoogle Scholar
  42. 42.
    Yokoi T, Yamashita S, Hibi T (2003) The nucleotide sequence and genome organization of Sclerophthora macrospora virus A. Virology 311:394–399CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018

Authors and Affiliations

  1. 1.Crop production and Pest Control Research Unit, ARS, USDA and Botany and Plant Pathology DepartmentPurdue UniversityWest LafayetteUSA
  2. 2.School of Integrative Plant ScienceCornell UniversityIthacaUSA
  3. 3.Department of Plant Biology and PathologyRutgers The State University of New JerseyNew BrunswickUSA

Personalised recommendations