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01-04-2018 | Original Article

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

Authors: B. Pandey, R. A. Naidu, G. G. Grove

Published in: Archives of Virology | Issue 4/2018

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.

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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 156:397–403PubMed

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 387:395–401PubMed

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 35:149–150

Anagnostakis SL (1982) Biological control of chestnut blight. Science 215(4532):466–471PubMed

Azzam OI, Gonsalves D (1991) Detection of dsRNA from cleistothecia and conidia of the grape powdery mildew pathogen Uncinula necator. Plant Dis 75:964–967

Braun U, Cook RTA (2012) Taxonomic Manual of the Erysiphales (Powdery Mildews). CBS Biodiver Ser 11:1–707

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 103:293–298PubMed

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 83:12801–12812PubMedPubMedCentral

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):2529–2534PubMedPubMedCentral

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 93:1407–1414PubMed

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 392:203–214PubMed

12.

Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedPubMedCentral

13.

Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118PubMed

14.

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

15.

Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368PubMed

16.

Grove GG (2004) Perennation of Uncinula necator in vineyards of Eastern Washington. Plant Dis 88:242–247PubMed

17.

Grove GG, Watson J (1996) Washington researchers attack powdery mildew. Good Fruit Grow 48(5):27–32

18.

Hadidi A, Flores R, Candresse T, Barba M (2016) Next-generation sequencing and genome editing in plant virology. Front Microbiol 7:1325PubMedPubMedCentral

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 6:175–192

20.

Hillman BI, Cai G (2013) The family Narnaviridae: simplest of RNA viruses. Adv Virus Res 86:149–176PubMed

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 1055–1060

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 10:252PubMedPubMedCentral

23.

Hollings M (1962) Viruses associated with a dieback disease of cultivated mushrooms. Nature 196:962–965

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 258:118–127PubMed

25.

Khalifa ME, Pearson MN (2013) Molecular characterization of three mitoviruses co-infecting a hypovirulent isolate of Sclerotinia sclerotiorum fungus. Virology 441:22–30PubMed

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 23–1208

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 213:353–364PubMed

28.

Lesker T, Rabenstein F, Maiss E (2013) Molecular characterization of five betacryp-toviruses infecting four clover species and dill. Arch Virol 158:1943–1952PubMed

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 154:565–572PubMed

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 108:111–119PubMed

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):e0154267PubMedPubMedCentral

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 104:660–666PubMed

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 105:135–140PubMed

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 188:90–96PubMed

35.

Morris TJ, Dodds JA (1979) Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858

36.

Mullins MG, Bouquet A, Williams LE (1992) Biology of the Grapevine. Cambridge University Press, New York, pp 1–241

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 188:128–141PubMed

38.

Nuss DL, Koltin Y (1990) Significance of dsRNA genetic elements in plant pathogenic fungi. Annu Rev Phytopathol 28:37–58PubMed

39.

Nuss DL (2005) Hypovirulence: mycoviruses at the fungal-plant interface. Nat Rev Microbiol 3(8):632–642PubMed

40.

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

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 2:15020PubMedPubMedCentral

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 93:1853–1868PubMedPubMedCentral

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 28:78–86PubMed

44.

Strauss EE, Lakshman DK, Tavantzis SM (2000) Molecular characterization of the genome of a partitivirus from the basidiomycete Rhizoctonia solani. J Gen Virol 81:549–555PubMed

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 9:28–39

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 22:4673–4680PubMedPubMedCentral

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 96:714–725PubMed

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 106:519–527PubMed

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 86:6605–6619PubMedPubMedCentral

50.

Wu MD, Zhang L, Li GQ, Jiang DH, Hou MS, Huang HC (2007) Hypovirulence and double-stranded RNA in Botrytis cinerea. Phytopathology 97:1590–1599PubMed

51.

Wu M, Zhang L, Li G, Jiang D, Ghabrial SA (2010) Genome characterization of a debilitation-associatedmitovirusinfectingthephytopathogenicfungus Botrytis cinerea. Virology 406(1):117–126PubMed

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 88:10120–10133PubMedPubMedCentral

53.

Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Ann Rev Phytopathol 52:45–68

54.

Xie J, Ghabrial SA (2012) Molecular characterizations of two mitoviruses co-infecting a hyovirulent isolate of the plant pathogenic fungus Sclerotinia sclerotiorum. Virology 428:77–85PubMed

55.

Xie J, Jiang D (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52:45–68PubMed

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 418:49–56PubMed

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 102:914–918

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 5:360PubMedPubMedCentral

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 456–457:220–226PubMed

Title: Detection and analysis of mycovirus-related RNA viruses from grape powdery mildew fungus Erysiphe necator
Authors: B. Pandey
R. A. Naidu
G. G. Grove
Publication date: 01-04-2018
Publisher: Springer Vienna
Published in: Archives of Virology / Issue 4/2018
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-018-3714-0

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