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Archives of Virology

, Volume 163, Issue 4, pp 1019–1030 | Cite as

Detection and analysis of mycovirus-related RNA viruses from grape powdery mildew fungus Erysiphe necator

  • B. PandeyEmail author
  • R. A. Naidu
  • G. G. Grove
Original Article

Abstract

The fungus, Erysiphe necator Schw., is an important plant pathogen causing powdery mildew disease in grapevines worldwide. In this study, high-throughput sequencing of double-stranded RNA extracted from the fungal tissue combined with bioinformatics was used to examine mycovirus-related sequences associated with E. necator. The results showed the presence of eight mycovirus-related sequences. Five of these sequences representing three new mycoviruses showed alignment with sequences of viruses classified in the genus Alphapartitivirus in the family Partitiviridae. Another three sequences representing three new mycoviruses showed similarity to classifiable members of the genus Mitovirus in the family Narnaviridae. These mycovirus isolates were named Erysiphe necator partitivirus 1, 2, and 3 (EnPV 1-3) and Erysiphe necator mitovirus 1, 2, and 3 (EnMV 1-3) reflecting their E. necator origin and their phylogenetic affiliation with other mycoviruses.

Notes

Compliance with Ethical Standards

This study was supported by Washington State University Agricultural Research Center.

Conflict of interest

First author B. Pandey declares he has no conflict of interest. Second author Naidu A. Rayapati declares he has no conflict of interest Third author Gary G. Grove declares he has no conflict of interest

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

705_2018_3714_MOESM1_ESM.docx (887 kb)
Supplementary material 1 (DOCX 887 kb)

References

  1. 1.
    Al Rwahnih M, Daubert S, Urbez-Torres JR, Cordero F, Rowhani A (2011) Deep sequencing evidence from single grapevine plants reveals a virome dominated by mycoviruses. Arch Virol 156:397–403CrossRefPubMedGoogle Scholar
  2. 2.
    Al Rwahnih M, Daubert S, Golino D, Rowhani A (2009) Deep sequence analysis of RNAs from grapevine showing Syrah decline symptoms reveals a multiple virus infection that includes a novel virus. Virology 387:395–401CrossRefPubMedGoogle Scholar
  3. 3.
    Amati A, Piva A, Castellari M, Arfelli G (1996) Preliminary studies on the effect of Oidium tuckeri on the phenolic composition of grapes and wines. Vitis 35:149–150Google Scholar
  4. 4.
    Anagnostakis SL (1982) Biological control of chestnut blight. Science 215(4532):466–471CrossRefPubMedGoogle Scholar
  5. 5.
    Azzam OI, Gonsalves D (1991) Detection of dsRNA from cleistothecia and conidia of the grape powdery mildew pathogen Uncinula necator. Plant Dis 75:964–967CrossRefGoogle Scholar
  6. 6.
    Braun U, Cook RTA (2012) Taxonomic Manual of the Erysiphales (Powdery Mildews). CBS Biodiver Ser 11:1–707Google Scholar
  7. 7.
    Candresse T, Marais A, Faure C, Gentit P (2013) Association of Little cherry virus 1 with the Shirofugen stunt disease and characterization of the genome of a divergent LChV1 isolate. Phytopathology 103:293–298CrossRefPubMedGoogle Scholar
  8. 8.
    Chiba S, Salaipeth L, Lin YH, Sasaki A, Kanematsu S, Suzuki N (2009) A novel bipartite double-stranded RNA mycovirus from the white root rot fungus Rosellinia necatrix: molecular and biological characterization, taxonomic considerations, and potential for biological control. J Virol 83:12801–12812CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Chu M, Jean J, Yea SJ, Kim YH, Lee YW, Kim KH (2002) Double-strand RNA mycoviruses from Fusarium graminearum. Appl Environ Microbiol 68(5):2529–2534CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Deng F, Xu R, Boland GJ (2003) Hypovirulence-associated double-stranded RNA from Sclerotinia homoeocarpa is conspecific with Ophiostoma novo-ulmi mitovirus 3a-Ld. Phytopathology 93:1407–1414CrossRefPubMedGoogle Scholar
  11. 11.
    Donaire L, Wang Y, Gonzalez-Ibeas D, Mayer KF, Aranda MA, Llave C (2009) Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology 392:203–214CrossRefPubMedGoogle Scholar
  12. 12.
    Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  14. 14.
    Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384CrossRefPubMedGoogle Scholar
  15. 15.
    Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368CrossRefPubMedGoogle Scholar
  16. 16.
    Grove GG (2004) Perennation of Uncinula necator in vineyards of Eastern Washington. Plant Dis 88:242–247CrossRefGoogle Scholar
  17. 17.
    Grove GG, Watson J (1996) Washington researchers attack powdery mildew. Good Fruit Grow 48(5):27–32Google Scholar
  18. 18.
    Hadidi A, Flores R, Candresse T, Barba M (2016) Next-generation sequencing and genome editing in plant virology. Front Microbiol 7:1325CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Hamby RK, Sims L, Issel L, Zimmer E (1988) Direct ribosomal RNA sequencing: optimization of extraction and sequencing methods for work with higher plants. Plant Mol Biol Report 6:175–192CrossRefGoogle Scholar
  20. 20.
    Hillman BI, Cai G (2013) The family Narnaviridae: simplest of RNA viruses. Adv Virus Res 86:149–176CrossRefPubMedGoogle Scholar
  21. 21.
    Hillman BI, Esteban R (2011) Narnaviridae. In: King AMQ, Adams, MJ, Carstens EB, Lefkowitz EJ (Eds.) Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier San Diego, pp 1055–1060Google Scholar
  22. 22.
    Hintz WE, Carneiro JS, Kassatenko I, Varga A, James D (2013) Two novel mitoviruses from a Canadian isolate of the Dutch elm pathogen Ophiostoma novo-ulmi. Virol J 10:252CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Hollings M (1962) Viruses associated with a dieback disease of cultivated mushrooms. Nature 196:962–965CrossRefGoogle Scholar
  24. 24.
    Hong Y, Dover SL, Cole TE, Brasier CM, Buck KW (1999) Multiple mitochondrial viruses in an isolate of the Dutch elm disease fungus Ophiostoma novo-ulmi. Virology 258:118–127CrossRefPubMedGoogle Scholar
  25. 25.
    Khalifa ME, Pearson MN (2013) Molecular characterization of three mitoviruses co-infecting a hypovirulent isolate of Sclerotinia sclerotiorum fungus. Virology 441:22–30CrossRefPubMedGoogle Scholar
  26. 26.
    King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (2012) Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses, vol 9. Elsevier Academic Press, London, pp 23–1208Google Scholar
  27. 27.
    Kondo H, Hisano S, Chiba S, Maruyama K, Andika IB, Toyoda K, Fujimori F, Suzuki N (2016) Sequence and phylogenetic analyses of novel totivirus-like double-stranded RNAs from field-collected powdery mildew fungi. Virus Res 213:353–364CrossRefPubMedGoogle Scholar
  28. 28.
    Lesker T, Rabenstein F, Maiss E (2013) Molecular characterization of five betacryp-toviruses infecting four clover species and dill. Arch Virol 158:1943–1952CrossRefPubMedGoogle Scholar
  29. 29.
    Li L, Tiam Q, Du Z, Duns GJ, Chen J (2009) A novel double stranded RNA virus detected in Primula malacoidesis a plant-isolated partitivirus closely related to partivirus infecting fungal species. Arch Virol 154:565–572CrossRefPubMedGoogle Scholar
  30. 30.
    Lim WS, Jeong JH, Jeong RD, Yoo YB, Yie SW, Kim KH (2005) Complete nucleotide sequence and genome organization of a dsRNA partitivirus infecting Pleurotus ostreatus. Virus Res 108:111–119CrossRefPubMedGoogle Scholar
  31. 31.
    Liu JJ, Chan D, Xiang Y, Williams H, Li XR, Sniezko RA, Sturrock RN (2016) Characterization of Five Novel Mitoviruses in the White Pine Blister Rust Fungus Cronartium ribicola. PLoS ONE 11(5):e0154267CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Marais A, Faure C, Couture C, Bergey B, Gentit P, Candresse T (2014) Characterization by deep sequencing of divergent Plum bark necrosis stem pitting virus isolates and development of a broad-spectrum PBNSPaV detection assay. Phytopathology 104:660–666CrossRefPubMedGoogle Scholar
  33. 33.
    Marais A, Faure C, Mustafayev E, Barone M, Alioto D, Candresse T (2015) Characterization by deep sequencing of Prunus virus T, a novel Tepovirus infecting Prunus species. Phytopathology 105:135–140CrossRefPubMedGoogle Scholar
  34. 34.
    Massart S, Olmos A, Jijakli H, Candresse T (2014) Current impact and future directions of high throughput sequencing in plant virus diagnostics. Virus Res 188:90–96CrossRefPubMedGoogle Scholar
  35. 35.
    Morris TJ, Dodds JA (1979) Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858CrossRefGoogle Scholar
  36. 36.
    Mullins MG, Bouquet A, Williams LE (1992) Biology of the Grapevine. Cambridge University Press, New York, pp 1–241Google Scholar
  37. 37.
    Nibert ML, Said SA, Ghabrial SA, Maiss E, Lesker T, Vainio EJ, Jiang D, Suzuki N (2014) Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res 188:128–141CrossRefPubMedGoogle Scholar
  38. 38.
    Nuss DL, Koltin Y (1990) Significance of dsRNA genetic elements in plant pathogenic fungi. Annu Rev Phytopathol 28:37–58CrossRefPubMedGoogle Scholar
  39. 39.
    Nuss DL (2005) Hypovirulence: mycoviruses at the fungal-plant interface. Nat Rev Microbiol 3(8):632–642CrossRefPubMedGoogle Scholar
  40. 40.
    Pearson MN, Beever RE, Boine B, Arthur K (2009) Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol 10:115–128CrossRefPubMedGoogle Scholar
  41. 41.
    Qiu W, Feechan A, Dry I (2015) Current understanding of grapevine defense mechanisms against the biotrophic fungus (Erysiphe necator), the causal agent of powdery mildew disease. Hortic Res 2:15020CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Radford AD, Chapman D, Dixon L, Chantrey J, Darby AC, Hall N (2012) Application of next-generation sequencing technologies in virology. J Gen Virol 93:1853–1868CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Schoebel CN, Zoller S, Rigling D (2014) Detection and genetic characterization of a novel mycovirus in Hymenoscyphus fraxineus, the causal agent of ash dieback. Infect Genet Evol 28:78–86CrossRefPubMedGoogle Scholar
  44. 44.
    Strauss EE, Lakshman DK, Tavantzis SM (2000) Molecular characterization of the genome of a partitivirus from the basidiomycete Rhizoctonia solani. J Gen Virol 81:549–555CrossRefPubMedGoogle Scholar
  45. 45.
    Stummer BE, Francis IL, Markides AJ, Scott ES (2003) The effect of powdery mildew infection of grape berries on juice and wine composition and on sensory properties of Chardonnay wines. Austr J Grape Wine Res 9:28–39CrossRefGoogle Scholar
  46. 46.
    Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTER W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Vainio EJ, Jurvansuu J, Streng J, Ki MR, Hantula J, Valkonen JPT (2015) Diagnosis and discovery of fungal viruses using deep sequencing of small RNAs. J Gen Virol 96:714–725CrossRefPubMedGoogle Scholar
  48. 48.
    Villamor DEV, Mekuria TA, Pillai SS, Eastwell KC (2016) High throughput sequencing identifies novel viruses in nectarine: insights to the etiology of stem pitting disease. Phytopathology 106:519–527CrossRefPubMedGoogle Scholar
  49. 49.
    Wu MD, Jin F, Zhang J, Yang L, Jiang D, Li G (2012) Characterization of a novel bipartite double-stranded RNA mycovirus conferring hypovirulence in the phytopathogenic fungus Botrytis porri. J Virol 86:6605–6619CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Wu MD, Zhang L, Li GQ, Jiang DH, Hou MS, Huang HC (2007) Hypovirulence and double-stranded RNA in Botrytis cinerea. Phytopathology 97:1590–1599CrossRefPubMedGoogle Scholar
  51. 51.
    Wu M, Zhang L, Li G, Jiang D, Ghabrial SA (2010) Genome characterization of a debilitation-associatedmitovirusinfectingthephytopathogenicfungus Botrytis cinerea. Virology 406(1):117–126CrossRefPubMedGoogle Scholar
  52. 52.
    Xiao X, Cheng J, Tang J, Fu Y, Jiang D, Baker TS, Ghabrial SA, Xie J (2014) A novel partitivirus that confers hypovirulence on plant pathogenic fungi. J Virol 88:10120–10133CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Ann Rev Phytopathol 52:45–68CrossRefGoogle Scholar
  54. 54.
    Xie J, Ghabrial SA (2012) Molecular characterizations of two mitoviruses co-infecting a hyovirulent isolate of the plant pathogenic fungus Sclerotinia sclerotiorum. Virology 428:77–85CrossRefPubMedGoogle Scholar
  55. 55.
    Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52:45–68CrossRefPubMedGoogle Scholar
  56. 56.
    Xie J, Xiao X, Fu Y, Liu H, Cheng J, Ghabrial SA, Li G, Jiang D (2011) A novel mycovirus closely related to hypoviruses that infects the plant pathogenic fungus Sclerotinia sclerotiorum. Virology 418:49–56CrossRefPubMedGoogle Scholar
  57. 57.
    Zabalgogeazcoa I, Benito EP, Ciudad AG, Criado BG, Eslava AP (1998) Double-stranded RNA and virus-like particles in the grass endophyte Epichloe festucae. Mycol Res 102:914–918CrossRefGoogle Scholar
  58. 58.
    Zhang R, Liu S, Chiba S, Kondo H, Kanematsu S, Suzuki N (2014) A novel single-stranded RNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix, with similarity to hypo-like viruses. Front Microbiol 5:360PubMedPubMedCentralGoogle Scholar
  59. 59.
    Zheng L, Zhang M, Chen Q, Zhu M, Zhou E (2014) A novel mycovirus closely related to viruses in the genus Alphapartitivirus confers hypovirulence in the phytopathogenic fungus Rhizoctonia solani. Virology 456–457:220–226CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Plant PathologyWashington State University, Irrigated Agriculture Research and Extension CenterProsserUSA
  2. 2.Department of Plant PathologyNorth Dakota State UniversityFargoUSA

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