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A novel victorivirus from the phytopathogenic fungus Neofusicoccum parvum

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Abstract

Neofusicoccum parvum is an important plant-pathogenic ascomycetous fungus that causes trunk diseases in a variety of plants. A limited number of reports on mycoviruses from this fungus are available. Here, we report the characterization of a novel victorivirus, Neofusicoccum parvum victorivirus 3 (NpVV3). An agarose gel dsRNA profile of a Pakistani strain of N. parvum, NFN, showed a band of ~5 kbp that was not detectable in Japanese strains of N. parvum. Taking a high-throughput and Sanger sequencing approach, the complete genome sequence of NpVV3 was determined to be 5226 bp in length with two open reading frames (ORF1 and ORF2) that encode a capsid protein (CP) and an RNA-dependent RNA polymerase (RdRP). The RdRP appears to be translated by a stop/restart mechanism facilitated by the junction sequence AUGucUGA, as is found in some other victoriviruses. BLASTp searches showed that NpVV3 CP and RdRP share the highest amino acid sequence identity (80.5% and 72.4%, respectively) with the corresponding proteins of NpVV1 isolated from a French strain of N. parvum. However, NpVV3 was found to be different from NpVV1 in its terminal sequences and the stop/restart facilitator sequence. NpVV3 particles ~35 nm in diameter were partially purified and used to infect an antiviral-RNA-silencing-deficient strain (∆dcl2) of an experimental ascomycetous fungal host, Cryphonectria parasitica. NpVV3 showed symptomless infection in the new host strain.

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Sequence data availability

The complete genomic nucleotide sequence of Neofusicoccum parvum victorivirus 3-NFN (NpVV3-NFN) was deposited in the GenBank/ENA/DDBJ database under accession number MZ868719.

References

  1. Aulia A, Andika IB, Kondo H, Hillman BI, Suzuki N (2019) A symptomless hypovirus, CHV4, facilitates stable infection of the chestnut blight fungus by a coinfecting reovirus likely through suppression of antiviral RNA silencing. Virology 533:99–107

    Article  CAS  Google Scholar 

  2. Chiapello M, Rodriguez-Romero J, Ayllon MA, Turina M (2020) Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages. Virus Evol 6:veaa058. https://doi.org/10.1093/ve/veaa1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 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 83:12801–12812

    Article  CAS  Google Scholar 

  4. Chiba S, Lin YH, Kondo H, Kanematsu S, Suzuki N (2013) A novel victorivirus from a phytopathogenic fungus, Rosellinia necatrix is infectious as particles and targeted by RNA silencing. J Virol 87:6727–6738

    Article  CAS  Google Scholar 

  5. Chiba Y, Oiki S, Yaguchi T, Urayama SI, Hagiwara D (2021) Discovery of divided RdRp sequences and a hitherto unknown genomic complexity in fungal viruses. Virus Evol 7:veaa101. https://doi.org/10.1093/ve/veaa1101

    Article  PubMed  Google Scholar 

  6. Criscuolo A, Gribaldo S (2010) BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 10:210

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Eusebio-Cope A, Suzuki N (2015) Mycoreovirus genome rearrangements associated with RNA silencing deficiency. Nucleic Acids Res 43:3802–3813

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  10. Guo LH, Sun L, Chiba S, Araki H, Suzuki N (2009) Coupled termination/reinitiation for translation of the downstream open reading frame B of the prototypic hypovirus CHV1-EP713. Nucleic Acids Res 37:3645–3659

    Article  CAS  Google Scholar 

  11. Jamal A, Sato Y, Shahi S, Shamsi W, Kondo H, Suzuki N (2019) Novel victorivirus from a Pakistani isolate of Alternaria alternata lacking a typical translational stop/restart sequence signature. Viruses 11:577

    Article  CAS  Google Scholar 

  12. Khan HA, Sato Y, Kondo H, Jamal A, Bhatti MF, Suzuki N (2021) A second capsidless hadakavirus strain with 10 positive-sense single-stranded RNA genomic segments from Fusarium nygamai. Arch Virol 166:2711–2722

    Article  CAS  Google Scholar 

  13. Khan HA, Shamsi W, Jamal A, Javaied M, Sadiq M, Fatma T, Ahmed A, Arshad M, Waseem M, Babar S, Dogar MM, Virk N, Janjua HA, Kondo H, Suzuki N, Bhatti MF (2021) Assessment of mycoviral diversity in Pakistani fungal isolates revealed infection by 11 novel viruses of a single strain of Fusarium mangiferae isolate SP1. J Gen Virol 102:001690. https://doi.org/10.1099/jgv.0.001690

  14. Kim JM, Jung JE, Park JA, Park SM, Cha BJ, Kim DH (2013) Biological function of a novel chrysovirus, CnV1-BS122, in the Korean Cryphonectria nitschkei BS122 strain. J Biosci Bioeng 115:1–3

    Article  CAS  Google Scholar 

  15. Li H, Havens WM, Nibert ML, Ghabrial SA (2011) RNA sequence determinants of a coupled termination-reinitiation strategy for downstream open reading frame translation in Helminthosporium victoriae virus 190S and other victoriviruses (Family Totiviridae). J Virol 85:7343–7352

    Article  CAS  Google Scholar 

  16. Li H, Havens WM, Nibert ML, Ghabrial SA (2015) An RNA cassette from Helminthosporium victoriae virus 190S necessary and sufficient for stop/restart translation. Virology 474:131–143

    Article  CAS  Google Scholar 

  17. Lin YH, Chiba S, Tani A, Kondo H, Sasaki A, Kanematsu S, Suzuki N (2012) A novel quadripartite dsRNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix. Virology 426:42–50

    Article  CAS  Google Scholar 

  18. Marais A, Faure C, Comont G, Candresse T, Stempien E, Corio-Costet MF (2021) Characterization of the mycovirome of the phytopathogenic fungus Neofusicoccum parvum. Viruses 13:375. https://doi.org/10.3390/v13030375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mata CP, Rodriguez JM, Suzuki N, Caston JR (2020) Structure and assembly of double-stranded RNA mycoviruses Virus assembly and exit pathways. Adv Virus Res 108:213–247

    Article  CAS  Google Scholar 

  20. Nerva L, Forgia M, Ciuffo M, Chitarra W, Chiapello M, Vallino M, Varese GC, Turina M (2019) The mycovirome of a fungal collection from the sea cucumber Holothuria polii. Virus Res 273:197737

    Article  CAS  Google Scholar 

  21. Nerva L, Turina M, Zanzotto A, Gardiman M, Gaiotti F, Gambino G, Chitarra W (2019) Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants. Environ Microbiol 21:2886–2904

    Article  CAS  Google Scholar 

  22. Preisig O, Wingfield BD, Wingfield MJ (1998) Coinfection of a fungal pathogen by two distinct double-stranded RNA viruses. Virology 252:399–406

    Article  CAS  Google Scholar 

  23. Romo M, Leuchtmann A, Garcia B, Zabalgogeazcoa I (2007) A totivirus infecting the mutualistic fungal endophyte Epichloe festucae. Virus Res 124:38–43

    Article  CAS  Google Scholar 

  24. Ruiz-Padilla A, Rodriguez-Romero J, Gomez-Cid I, Pacifico D, Ayllon MA (2021) Novel mycoviruses discovered in the mycovirome of a necrotrophic fungus. MBio 12:e03705-03720. https://doi.org/10.01128/mBio.03705-03720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sato Y, Shamsi W, Jamal A, Bhatti MF, Kondo H, Suzuki N (2020) Hadaka virus 1: a capsidless eleven-segmented positive-sense single-stranded RNA virus from a phytopathogenic fungus Fusarium oxysporum. MBio 11:e00450–e001420. https://doi.org/10.01128/mBio.00450-00420

    Article  PubMed  PubMed Central  Google Scholar 

  26. Segers GC, Zhang X, Deng F, Sun Q, Nuss DL (2007) Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. Proc Natl Acad Sci U S A 104:12902–12906

    Article  CAS  Google Scholar 

  27. Shahi S, Eusebio-Cope A, Kondo H, Hillman BI, Suzuki N (2019) Investigation of host range of and host defense against a mitochondrially replicating mitovirus. J Virol 93:e01503-01518

    Article  CAS  Google Scholar 

  28. Shamsi W, Sato Y, Jamal A, Shahi S, Kondo H, Suzuki N, Bhatti MF (2019) Molecular and biological characterization of a novel botybirnavirus identified from a Pakistani isolate of Alternaria alternata. Virus Res 263:119–128

    Article  CAS  Google Scholar 

  29. Sun L, Suzuki N (2008) Intragenic rearrangements of a mycoreovirus induced by the multifunctional protein p29 encoded by the prototypic hypovirus CHV1-EP713. RNA 14:2557–2571

    Article  CAS  Google Scholar 

  30. Sutela S, Poimala A, Vainio EJ (2019) Viruses of fungi and oomycetes in the soil environment. FEMS Microbiol Ecol 95:fiz119. https://doi.org/10.1093/femsec/fiz119

  31. Sutela S, Forgia M, Vainio EJ, Chiapello M, Daghino S, Vallino M, Martino E, Girlanda M, Perotto S, Turina M (2020) The virome from a collection of endomycorrhizal fungi reveals new viral taxa with unprecedented genome organization. Virus Evol 6:veaa076

    Article  Google Scholar 

  32. Suzuki N (2021) An introduction to fungal viruses. In: Bamford D, Zuckerman M (eds) Encyclopedia of virology, 4th edn. Elsevier, Oxford, pp 431–442. https://doi.org/10.1016/B1978-1010-1012-814515-814519.800045-X

    Chapter  Google Scholar 

  33. Telengech P, Hisano S, Mugambi C, Hyodo K, Arjona-Lopez JM, Lopez-Herrera CJ, Kanematsu S, Kondo H, Suzuki N (2020) Diverse partitiviruses from the phytopathogenic fungus Rosellinia necatrix. Front Microbiol 11(1064):10. https://doi.org/10.3389/fmicb.2020.01064

    Article  Google Scholar 

  34. Urayama S, Katoh Y, Fukuhara T, Arie T, Moriyama H, Teraoka T (2015) Rapid detection of Magnaporthe oryzae chrysovirus 1-A from fungal colonies on agar plates and lesions of rice blast. J Gen Plant Pathol 81:97–102

    Article  Google Scholar 

  35. Wickner RB, Ghabrial SA, Nibert ML, Patterson JL, Wang CC (2011) Family Totiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowits EJ (eds) Virus taxonomy: ninth report of the international committee for the taxonomy of viruses. Elsevier, Academic Press, New York, pp 639–650

    Google Scholar 

  36. Xie J, Havens WM, Lin YH, Suzuki N, Ghabrial SA (2016) The victorivirus Helminthosporium victoriae virus 190S is the primary cause of disease/hypovirulence in its natural host and a heterologous host. Virus Res 213:238–245

    Article  CAS  Google Scholar 

  37. Yang MM, Zhai LF, Xiao F, Guo YS, Fu M, Hong N, Wang GP (2019) Characterization of a novel victorivirus isolated from the phytopathogenic fungus Botryosphaeria dothidea. Arch Virol 164:1609–1617

    Article  CAS  Google Scholar 

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Acknowledgements

HAK is thankful to the Higher Education Commission (HEC) of Pakistan for a fellowship under the International Research Support Initiative Program (IRSIP). YS is a JSPS (Japan Society for the Promotion of Science) fellow. The authors are grateful to Dr. Donald L. Nuss for the generous gift of C. parasitica strain ∆dcl2. The authors are also grateful to Dr. Sabitree Shahi and Ms. Sakae Hisano for technical assistance.

Funding

This study was supported in part by Yomogi Inc., the Ohara Foundation for Agriculture Research (to NS), and Grants-in-Aid for Scientific Research on Innovative Areas from the Japanese Ministry of Education, Culture, Sports, Science and Technology (KAKENHI 21H05035, 17H01463, 16H06436, 16H06429 and 16K21723 to N.S. and H.K.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. Atta-ur-Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), H-12, Islamabad, 44000, Pakistan

    Haris Ahmed Khan & Muhammad Faraz Bhatti

  2. Institute of Plant Science and Resources, Okayama University, Kurashiki, 710-0046, Japan

    Haris Ahmed Khan, Yukiyo Sato, Hideki Kondo & Nobuhiro Suzuki

  3. Crop Diseases Research Institute, National Agricultural Research Centre, Islamabad, Pakistan

    Atif Jamal

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  1. Haris Ahmed Khan
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Correspondence to Nobuhiro Suzuki.

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Supplementary Information

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705_2021_5304_MOESM1_ESM.pdf

Supplementary Fig. S1 Multiple alignment of the amino acid sequences of the conserved motifs in RdRps of NpVV3 and other victoriviruses. Virus names and abbreviations are as follows: NpVV3, Neofusicoccum parvum victorivirus 3 (accession no. MZ868719); NpVV1, Neofusicoccum parvum victorivirus 1 (accession no. QTE76048.1); RnVV1, Rosellinia necatrix victorivirus 1 (accession no. YP_008130308.1); UvRV1, Ustilaginoidea virens RNA virus 1 (accession no.YP_007761589.1); MpVV1, Macrophomina phaseolina victorivirus 1 (accession no. QKI37143.1); PlTV1, Phomopsis longicolla totivirus 1 (accession no. ALD89108.1); AaVV1, Alternaria arborescens victorivirus 1 (accession no. YP_009553478.1); CmRV, Coniothyrium minitans RNA virus (accession no. YP_392467.1); PdV1, Penicillium digitatum virus 1 (accession no. AMY26886.1); MoV2, Magnaporthe oryzae virus 2 (accession no. BBG92298.1); SsRV2, Sphaeropsis sapinea RNA virus 2 (accession no. NP_047560.1); UvRV1, Ustilaginoidea virens RNA virus 1 (accession no. YP_007761589.1) (PDF 597 KB)

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Khan, H.A., Sato, Y., Kondo, H. et al. A novel victorivirus from the phytopathogenic fungus Neofusicoccum parvum. Arch Virol 167, 923–929 (2022). https://doi.org/10.1007/s00705-021-05304-7

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