Skip to main content
SpringerLink
Log in

Characterization of a novel dsRNA mycovirus of Trichoderma atroviride NFCF377 reveals a member of “Fusagraviridae” with changes in antifungal activity of the host fungus

  • Microbial Genetics, Genomics and Molecular Biology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Trichoderma atroviride is a common fungus found in various ecosystems that shows mycoparasitic ability on other fungi. A novel dsRNA virus was isolated from T. atroviride NFCF377 strain and its molecular features were analyzed. The viral genome consists of a single segmented double-stranded RNA and is 9,584 bp in length, with two discontinuous open reading frames (ORF1 and ORF2). A mycoviral structural protein and an RNA-dependent RNA polymerase (RdRp) are encoded by ORF1 and ORF2, respectively, between which is found a canonical shifty heptameric signal motif (AAAAAAC) followed by an RNA pseudoknot. Analysis of sequence similarity and phylogeny showed that it is closely related to members of the proposed family “Fusagraviridae”, with a highest similarity to the Trichoderma atroviride mycovirus 1 (TaMV1). Although the sequence similarity of deduced amino acid to TaMV1 was evident, sequence deviations were distinctive at untranslated regions (UTRs) due to the extended size. Thus, we inferred this dsRNA to be a different strain of Trichoderma atroviride mycovirus 1 (TaMV1-NFCF377). Electron microscopy image exhibited an icosahedral viral particle of 40 nm diameter. Virus-cured isogenic isolates were generated and no differences in growth rate, colony morphology, or conidia production were observed between virus-infected and virus-cured strains. However, culture filtrates of TaMV1-NFCF377-infected strain showed enhanced antifungal activity against the plant pathogen Rhizoctonia solani but not to edible mushroom Pleurotus ostreatus. These results suggested that TaMV1-NFCF377 affected the metabolism of the fungal host to potentiate antifungal compounds against a plant pahogen, but this enhanced antifungal activity appeared to be species-specific.

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

Similar content being viewed by others

References

  • Ahn, I.P. and Lee, Y.H. 2001. A viral double-stranded RNA up regulates the fungal virulence of Nectria radicicola. Mol. Plant Microbe Interact. 14, 496–507.

    CAS  PubMed  Google Scholar 

  • Andika, I.B., Wei, S., Cao, C., Salaipeth, L., Kondo, H., and Sun, L. 2017. Phytopathogenic fungus hosts a plant virus: A naturally occurring cross-kingdom viral infection. Proc. Natl. Acad. Sci. USA 114, 12267–12272.

    CAS  PubMed  Google Scholar 

  • Anfoka, C. and Buchenauer, H. 1997. Systemic acquired resistance in tomato against Phytophthora infestans by pre-inoculation with tobacco necrosis virus. Physiol. Mol. Plant Pathol. 50, 85–101.

    CAS  Google Scholar 

  • Arjona-Lopez, J.M., Telengech, P., Jamal, A., Hisano, S., Kondo, H., Yelin, M.D., Arjona-Girona, I., Kanematsu, S., Lopez-Herrera, C.J., and Suzuki, N. 2018. Novel, diverse RNA viruses from Mediterranean isolates of the phytopathogenic fungus, Rosellinia necatrix: insights into evolutionary biology of fungal viruses. Environ. Microbiol. 20, 1464–1483.

    CAS  PubMed  Google Scholar 

  • Asad, S.A., Ali, N., Hameed, A., Khan, S.A., Ahmad, R., Bilal, M., Shahzad, M., and Tabassum, A. 2014. Biocontrol efficacy of different isolates of Trichoderma against soil borne pathogen Rhizoctonia solani. Pol. J. Microbiol. 63, 95–103.

    PubMed  Google Scholar 

  • Bidet, K. and Garcia-Blanco, M.A. 2014. Flaviviral RNAs: weapons and targets in the war between virus and host. Biochem. J. 462, 215–230.

    CAS  PubMed  Google Scholar 

  • Brierley, I. 1995. Ribosomal frameshifting on viral RNAs. J. Gen. Virol. 76, 1885–1892.

    CAS  PubMed  Google Scholar 

  • Brierley, I., Pennell, S., and Gilbert, R.J.C. 2007. Viral RNA pseudoknots: versatile motifs in gene expression and replication. Nat. Rev. Microbiol. 5, 598–610.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chun, J., Yang, H.E., and Kim, D.H. 2018a. Identification and molecular characterization of a novel partitivirus from Trichoderma atroviride NFCF394. Viruses 10, 578.

    CAS  PubMed Central  Google Scholar 

  • Chun, J., Yang, H.E., and Kim, D.H. 2018b. Identification of a novel partitivirus of Trichoderma harzianum NFCF319 and evidence for the related antifungal activity. Front. Plant Sci. 9, 1699.

    PubMed  PubMed Central  Google Scholar 

  • Coninck, E., Scauflaire, J., Gollier, M., Liénard, C., Foucart, G., Manssens, G., Munaut, F., and Legrève, A. 2020. Trichoderma atroviride as a promising biocontrol agent in seed coating for reducing Fusarium damping-off on maize. J. Appl. Microbiol. 129, 637–651.

    CAS  PubMed  Google Scholar 

  • Dennis, C. and Webster, J. 1971. Antagonistic properties of species-groups of Trichoderma: II. Production of volatile antibiotics. Trans. Br. Mycol. Soc. 57, 41–48.

    CAS  Google Scholar 

  • de Sá, P.B., Havens, W.M., and Ghabrial, S.A. 2010. Characterization of a novel broad-spectrum antifungal protein from virus-infected Helminthosporium (Cochliobolus) victoriae. Phytopathology 100, 880–889.

    PubMed  Google Scholar 

  • Eusebio-Cope, A., Sun, L., Tanaka, T., Chiba, S., Kasahara, S., and Suzuki, N. 2015. The chestnut blight fungus for studies on virus/host and virus/virus interactions: from a natural to a model host. Virology 477, 164–175.

    CAS  PubMed  Google Scholar 

  • Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.

    PubMed  Google Scholar 

  • Gebhard, L.G., Filomatori, C.V., and Gamarnik, A.V. 2011. Functional RNA elements in the dengue virus genome. Viruses 3, 1739–1756.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghabrial, S.A., Castón, J.R., Jiang, D., Nibert, M.L., and Suzuki, N. 2015. 50-plus years of fungal viruses. Virology 479–480, 356–368.

    PubMed  Google Scholar 

  • Ghabrial, S.A. and Suzuki, N. 2009. Viruses of plant pathogenic fungi. Annu. Rev. Phytopathol. 47, 353–384.

    CAS  PubMed  Google Scholar 

  • Gomes, R.C., Sêmedo, L.T.A.S., Soares, R.M.A., Linhares, L.F., Ulhoa, C.J., Alviano, C.S., and Coelho, R.R. 2001. Purification of a thermostable endochitinase from Streptomyces RC1071 isolated from a cerrado soil and its antagonism against phytopathogenic fungi. J. Appl. Microbiol. 90, 653–661.

    CAS  PubMed  Google Scholar 

  • Kanhayuwa, L., Kotta-Loizou, I., Özkan, S., Gunning, A.P., and Coutts, R.H.A. 2015. A novel mycovirus from Aspergillus fumigatus contains four unique dsRNAs as its genome and is infectious as dsRNA. Proc. Natl. Acad. Sci. USA 112, 9100–9105.

    CAS  PubMed  Google Scholar 

  • Kim, J.M., Jung, J.E., Park, J.A., Park, S.M., Cha, B.J., and Kim, D.H. 2013. Biological function of a novel chrysovirus, CnV1-BS122, in the Korean Cryphonectria nitschkei BS122 strain. J. Biosci. Bioeng. 115, 1–3.

    CAS  PubMed  Google Scholar 

  • Kombrink, E. and Somssich, I.E. 1997. Pathogenesis-related proteins and plant defense. In Carroll, G.C. and Tudzynski, P. (eds.), The Mycota: A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research, vol. 5, pp. 107–128. Springer, Berlin, Germany.

    Google Scholar 

  • Kotta-Loizou, I. and Coutts, R.H.A. 2017. Studies on the virome of the entomopathogenic fungus Beauveria bassiana reveal novel dsRNA elements and mild hypervirulence. PLoS Pathog. 13, e1006183.

    PubMed  PubMed Central  Google Scholar 

  • Kumar, S., Stecher, G., and Tamura, K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.

    CAS  Google Scholar 

  • Lee, S.H., Yun, S.H., Chun, J., and Kim, D.H. 2017. Characterization of a novel dsRNA mycovirus of Trichoderma atroviride NFCF028. Arch. Virol. 162, 1073–1077.

    CAS  PubMed  Google Scholar 

  • Meena, M., Swapnil, P., Zehra, A., Dubey, M.K., and Upadhyay, R.S. 2017. Antagonistic assessment of Trichoderma spp. by producing volatile and non-volatile compounds against different fungal pathogens. Arch. Phytopathol. Plant Prot. 50, 629–648.

    CAS  Google Scholar 

  • Nakamura, H., Ikeda, K., Arakawa, M., and Matsumoto, N. 2002. Conidioma production of the white root rot fungus in axenic culture under near-ultraviolet light radiation. Mycoscience 43, 251–254.

    Google Scholar 

  • Nawrocka, J., Gromek, A., and Malolepsza, U. 2019. Nitric oxide as a beneficial signaling molecule in Trichoderma atroviride TRS25-induced systemic defense responses of cucumber plants against Rhizoctonia solani. Front. Plant Sci. 10, 421.

    PubMed  PubMed Central  Google Scholar 

  • Nuss, D.L. 2005. Hypovirulence: mycoviruses at the fungal-plant interface. Nat. Rev. Microbiol. 3, 632–642.

    CAS  PubMed  Google Scholar 

  • Park, S.M., Choi, E.S., Kim, M.J., Cha, B.J., Yang, M.S., and Kim, D.H. 2004. Characterization of HOG1 homologue, CpMK1, from Cryphonectria parasitica and evidence for hypovirus-mediated perturbation of its phosphorylation in response to hypertonic stress. Mol. Microbiol. 51, 1267–1277.

    CAS  PubMed  Google Scholar 

  • Park, S.M., Kim, J.M., Chung, H.J., Lim, J.Y., Kwon, B.R., Lim, J.G., Kim, J.A., Kim, M.J., Cha, B.J., Lee, S.H., et al. 2008. Occurrence of diverse dsRNA in a Korean population of the chestnut blight fungus, Cryphonectria parasitica. Mycol. Res. 112, 1220–1226.

    CAS  PubMed  Google Scholar 

  • Polacheck, I. and Rosenberger, R.F. 1978. Distribution of autolysins in hyphae of Aspergillus nidulans: evidence for a lipid-mediated attachment to hyphal walls. J. Bacteriol. 135, 741–747.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seaby, D. 1998. Trichoderma as a weed mould or pathogen in mushroom cultivation. In Harman, G.E. and Kubicek, C.P. (eds.), Trichoderma and Gliocladium. vol. 2, pp. 267–288. Taylor & Francis, London, the United Kingdom.

    Google Scholar 

  • Stoppacher, N., Kluger, B., Zeilinger, S., Krska, R., and Schuhmacher, R. 2010. Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J. Microbiol. Methods 81, 187–193.

    CAS  PubMed  Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, L., Jiang, J., Wang, Y., Hong, N., Zhang, F., Xu, W., and Wang, G. 2014. Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus. J. Virol. 88, 7517–7527.

    PubMed  PubMed Central  Google Scholar 

  • Wang, L., Zhang, J., Zhang, H., Qiu, D., and Guo, L. 2016. Two novel relative double-stranded RNA mycoviruses infecting Fusarium poae strain SX63. Int. J. Mol. Sci. 17, 641.

    PubMed Central  Google Scholar 

  • Weiler, F., Rehfeldt, K., Bautz, F., and Schmitt, M.J. 2002. The Zygosaccharomyces bailii antifungal virus toxin zygocin: cloning and expression in a heterologous fungal host. Mol. Microbiol. 46, 1095–1105.

    CAS  PubMed  Google Scholar 

  • Wheatley, R., Hackett, C., Bruce, A., and Kundzewicz, A. 1997. Effect of substrate composition on production of volatile organic compounds from Trichoderma spp. inhibitory to wood decay fungi. Int. Biodeterior. Biodegradation 39, 199–205.

    CAS  Google Scholar 

  • Wickner, R.B. 1992. Double-stranded and single-stranded RNA viruses of Saccharomyces cerevisiae. Annu. Rev. Microbiol. 46, 347–375.

    CAS  PubMed  Google Scholar 

  • Wu, M.D., Jin, F.Y., Zhang, J., Yang, L., Jiang, D., and Li, G. 2012. Characterization of a novel bipartite double-stranded RNA mycovirus conferring hypovirulence in the phytopathogenic fungus Botrytis porri. J. Virol. 86, 6605–6619.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yun, S.H., Lee, S.H., So, K.K., Kim, J.M., and Kim, D.H. 2016. Incidence of diverse dsRNA mycoviruses in Trichoderma spp. causing green mold disease of shiitake Lentinula edodes. FEMS Microbiol. Lett. 363, fnw220.

    PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank the Institute of Molecular Biology and Genetics at Jeonbuk National University for kindly providing the facilities for this research. This work was supported by the NRF grants from NRF-2018R1A2A1A05078682 and NRF-2019R1I1A1A01061618. This research was supported by “Research Base Construction Fund Support Program” funded by Jeonbuk National University in 2020.

Author information

Authors and Affiliations

  1. Institute for Molecular Biology and Genetics, Jeonbuk National University, Jeonju, 54896, Republic of Korea

    Jeesun Chun & Dae-Hyuk Kim

  2. Department of Bioactive Material Sciences, Jeonbuk National University, Jeonju, 54896, Republic of Korea

    Byeonghak Na & Dae-Hyuk Kim

  3. Department of Molecular Biology, Jeonbuk National University, Jeonju, 54896, Republic of Korea

    Dae-Hyuk Kim

Authors
  1. Jeesun Chun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Byeonghak Na
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dae-Hyuk Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dae-Hyuk Kim.

Additional information

Conflict of Interest

Authors declare no competing interests.

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chun, J., Na, B. & Kim, DH. Characterization of a novel dsRNA mycovirus of Trichoderma atroviride NFCF377 reveals a member of “Fusagraviridae” with changes in antifungal activity of the host fungus. J Microbiol. 58, 1046–1053 (2020). https://doi.org/10.1007/s12275-020-0380-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-020-0380-1

Keywords

Search

Navigation