Skip to main content
SpringerLink
Log in

Characterization of two novel fusariviruses co-infecting a single isolate of phytopathogenic fungus Botrytis cinerea

  • Original Paper
  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

A wide diversity of mycoviruses has been reported from Botrytis species, some with the potential to suppress the pathogenic abilities of this fungus. Considering their importance, this study was devised to find potential hypovirulence-associated mycoviruses found in Botrytis cinerea strains isolated from Pakistani strawberry fields. Here we report the complete genome characterization of two fusariviruses co-infecting a single isolate of phytopathogenic fungus B. cinerea (Kst14a). The viral genomes were sequenced by deep sequencing using total RNA fractions of the Kst14a isolate. The identified viruses were tentatively named Botrytis cinerea fusarivirus 9 (BcFV9) and Botrytis cinerea fusarivirus 3a (BcFV3a). Both viruses had a single-segmented (ssRNA) genome having a size of 6424 and 8370 nucleotides encoding two discontinuous open reading frames (ORFs). ORF-1 of both mycoviruses encodes for a polyprotein having a conserved domain of RNA-dependent RNA polymerase (RdRP) and a helicase domain (Hel) which function in RNA replication, while ORF2 encodes a hypothetical protein with an unknown function, respectively. Phylogenetic analysis indicated that BcFV9 made a clade with the genus Alphafusarivirus and BcFV3a fall in the genus Betafusarivirus in the family Fusariviridae. To our knowledge, this is the first report of two fusariviruses identified in isolates of B. cinerea from Pakistan. Both mycoviruses successfully transfected to a compatible strain of B. cinerea (Mst11). A comparison of virus-free (VF) and virus-infected (VI) isogenic lines showed the presence of these viruses was causing hypovirulence in infected strains. Virus-infected strains also had a small lesion size while testing the pathogenicity via apple assay.

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

Similar content being viewed by others

Data availability

The genome sequence mentioned in this study can be found under the accession codes OK558541.1 and OK558542.1. The names of the repository/repositories and accession number(s) can be found in the Manuscript/Supplementary Material.

References

  1. Ruiz-Padilla A, Rodríguez-Romero J, Gómez-Cid I, Pacifico D, Ayllón MA (2021) Novel mycoviruses discovered in the mycovirome of a necrotrophic fungus. MBio 12(3):10–1128

    Article  Google Scholar 

  2. Liu L, Xie J, Cheng J, Fu Y, Li G, Yi X, Jiang D (2014) Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses. Proc Natl Acad Sci 111(33):12205–12210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lin YH, Fujita M, Chiba S, Hyodo K, Andika IB, Suzuki N, Kondo H (2019) Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes). Virology 533:125–136

    Article  CAS  PubMed  Google Scholar 

  4. Feng C, Feng J, Wang Z, Pedersen C, Wang X, Saleem H et al (2021) Identification of the viral determinant of hypovirulence and host range in Sclerotiniaceae of a genomovirus reconstructed from the plant metagenome. J Virol 95(17):10–1128

    Article  Google Scholar 

  5. 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 5:360

    Article  PubMed  PubMed Central  Google Scholar 

  6. Picarelli MAS, Forgia M, Rivas EB, Nerva L, Chiapello M, Turina M, Colariccio A (2019) Extreme diversity of mycoviruses present in isolates of Rhizoctonia solani AG2-2 LP from Zoysia japonica from Brazil. Front Cell Infect Microbiol 9:244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Petrasch S, Knapp SJ, Van Kan JA, Blanco-Ulate B (2019) Grey mould of strawberry, a devastating disease caused by the ubiquitous necrotrophic fungal pathogen Botrytis cinerea. Mol Plant Pathol 20(6):877–892

    Article  PubMed  PubMed Central  Google Scholar 

  8. Romanazzi G, Smilanick JL, Feliziani E, Droby S (2016) Integrated management of postharvest gray mold on fruit crops. Postharvest Biol Technol 113:69–76

    Article  CAS  Google Scholar 

  9. Wu M, Zhang J, Yang L, Li G (2015) RNA mycoviruses and their role in Botrytis biology. Botrytis—the fungus, the pathogen and its management in agricultural systems. Springer, pp 71–90

    Google Scholar 

  10. Pearson MN, Bailey AM (2013) Viruses of botrytis. Adv Virus Res 86:249–272

    Article  PubMed  Google Scholar 

  11. Wu M, 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(12):6605–6619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Yu L, Sang W, Wu MD, Zhang J, Yang L, Zhou YJ et al (2015) Novel hypovirulence-associated RNA mycovirus in the plant-pathogenic fungus Botrytis cinerea: molecular and biological characterization. Appl Environ Microbiol 81(7):2299–2310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Donaire L, Rozas J, Ayllón MA (2016) Molecular characterization of Botrytis ourmia-like virus, a mycovirus close to the plant pathogenic genus Ourmiavirus. Virology 489:158–164

    Article  CAS  PubMed  Google Scholar 

  14. Donaire L, Pagán I, Ayllón MA (2016) Characterization of Botrytis cinerea negative-stranded RNA virus 1, a new mycovirus related to plant viruses, and a reconstruction of host pattern evolution in negative-sense ssRNA viruses. Virology 499:212–218

    Article  CAS  PubMed  Google Scholar 

  15. Wu MD, Zhang L, Li GQ, Jiang DH, Hou MS, Huang HC (2007) Hypovirulence and double-stranded RNA in Botrytis cinerea. Phytopathology 97(12):1590–1599

    Article  CAS  PubMed  Google Scholar 

  16. Wu M, Zhang L, Li G, Jiang D, Ghabrial SA (2010) Genome characterization of a debilitation-associated mitovirus infecting the phytopathogenic fungus Botrytis cinerea. Virology 406(1):117–126

    Article  CAS  PubMed  Google Scholar 

  17. Eusebio-Cope A, Suzuki N (2015) Mycoreovirus genome rearrangements associated with RNA silencing deficiency. Nucleic Acids Res 43(7):3802–3813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bhatti MF, Bignell EM, Coutts RHA (2011) Complete nucleotide sequences of two dsRNAs associated with a new partitivirus infecting Aspergillus fumigatus. Arch Virol 156:1677–1680

    Article  CAS  PubMed  Google Scholar 

  19. Potgieter CA, Castillo A, Castro M, Cottet L, Morales A (2013) A wild-type Botrytis cinerea strain co-infected by double-stranded RNA mycoviruses presents hypovirulence-associated traits. Virol J 10(1):1–9

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  21. Gong W, Liu H, Zhu X, Zhao S, Cheng J, Zhu H et al (2021) Molecular characterization of a novel fusarivirus infecting the plant-pathogenic fungus Alternaria solani. Adv Virol 166(7):2063–2067

    CAS  Google Scholar 

  22. 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. Adv Virol 166:2711–2722

    CAS  Google Scholar 

  23. Hrabáková L, Grum-Grzhimaylo AA, Koloniuk I, Debets AJ, Sarkisova T, Petrzik K (2017) The alkalophilic fungus Sodiomyces alkalinus hosts beta-and gammapartitiviruses together with a new fusarivirus. PLoS ONE 12(11):e0187799

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ahmed A, Khan HA, Jamal A, Baig DI, Fatma T, Virk N, Bhatti MF (2023) The presence of mycoviral infection attenuates the growth and pathogenicity of the phytopathogenic fungus Botrytis cinerea collected from strawberry fields in Pakistan. Eur J Plant Pathol 167:133–143

    Article  CAS  Google Scholar 

  25. Gao F, Anane RF, Liu Z, Zi S, Li S, Yang Z et al (2023) Complete genome sequence of a novel fusarivirus from the phytopathogenic fungus Fusarium sp. Adv Virol 168(10):248

    CAS  Google Scholar 

  26. 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(5):2529–2534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wang Q, Zou Q, Dai Z, Hong N, Wang G, Wang L (2022) Four novel mycoviruses from the hypovirulent Botrytis cinerea SZ-2-3y isolate from Paris polyphylla: molecular characterisation and mitoviral sequence transboundary entry into plants. Viruses 14(1):151

    Article  PubMed  PubMed Central  Google Scholar 

  28. Zhang L, Chen X, Bhattacharjee P, Shi Y, Guo L, Wang S (2020) Molecular characterization of a novel strain of Fusarium graminearum virus 1 infecting Fusarium graminearum. Viruses 12(3):357

Download references

Acknowledgements

This work was supported by the funding of NRPU (Research Grant No. 20-4109/R&D/HEC/14/847) awarded to MFB and NV), and the research was carried out in Fungal Infections & Virology Group (FIV-G), ASAB, NUST with the collaboration of Aflatoxin Lab, CDRI, NARC.

Author information

Authors and Affiliations

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

    Aqeel Ahmed, Haris Ahmed Khan, Nasar Virk & Muhammad Faraz Bhatti

  2. Department of Biotechnology, University of Mianwali, Punjab, 42200, Pakistan

    Haris Ahmed Khan

  3. Crop Disease Research Institute (CDRI), National Agricultural Research Centre (NARC), Islamabad, Pakistan

    Atif Jamal

  4. EBS Business School, EBS Universität für Wirtschaft und Recht, Rheingaustrasse 1, 65375, Oestrich-Winkel, Germany

    Nasar Virk

Authors
  1. Aqeel Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haris Ahmed Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Atif Jamal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nasar Virk
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad Faraz Bhatti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muhammad Faraz Bhatti.

Ethics declarations

Conflict of interest

All authors declare that they have no conflicts of interest.

Ethical approval

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

Additional information

Edited by Maija Pollari.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

11262_2024_2073_MOESM1_ESM.jpg

Supplementary file1 (JPG 29 KB) Colony morphology and transmission assay of the virus from infected (+) isolate Kst14 (designated as D for Donor) to uninfected isolate (−) Mst11 (designated as R for Recipient). Both viruses successfully transferred to the recipient strain

Supplementary file2 (DOCX 13 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmed, A., Khan, H.A., Jamal, A. et al. Characterization of two novel fusariviruses co-infecting a single isolate of phytopathogenic fungus Botrytis cinerea. Virus Genes (2024). https://doi.org/10.1007/s11262-024-02073-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11262-024-02073-8

Keywords

Search

Navigation