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Journal of General Virology header logo Journal of General Virology

Volume 104, Issue 8

New viruses of sp. expand considerably the taxonomic structure of genus Open Access

Abstract

Despite the fact that sp. are ubiquitous fungi, their viromes have been little studied. By analysing a collection of fungi, two new partitiviruses named Cladosporium cladosporioides partitivirus 1 (CcPV1) and Cladosporium cladosporioides partitivirus 2 (CcPV2) co-infecting a strain of were identified. Their complete genome consists of two monocistronic dsRNA segments (RNA1 and RNA2) with a high percentage of pairwise identity on 5′ and 3′ end. The RNA directed RNA polymerase (RdRp) of both viruses and the capsid protein (CP) of CcPV1 display the classic characteristics required for their assignment to the genus. In contrast, CcPV2 RNA2 encodes for a 41 KDa CP that is unusually smaller when aligned to CPs of other viruses classified in this genus. The structural role of this protein is confirmed by electrophoresis on acrylamide gel of purified viral particles. Despite the low percentage of identity between the capsid proteins of CcPV1 and CcPV2, their three-dimensional structures predicted by AlphaFold2 show strong similarities and confirm functional proximity. Fifteen similar viral sequences of unknown function were annotated using the CcPV2 CP sequence. The phylogeny of the CP was highly consistent with the phylogeny of their corresponding RdRp, supporting the organization of into three distinct clades despite stretching the current demarcation criteria. It is proposed that a new subgenus be created within the genus Gammapartitivirus for this new group.

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Keyword(s): Cladosporium , Gammapartitivirus , mycovirus , taxonomy and VANA
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-08-07
2025-06-19
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References

  1. Porras-Alfaro A, Bayman P. Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 2011; 49:291–315 [View Article] [PubMed]
     [Google Scholar]
  2. Belda I, Zarraonaindia I, Perisin M, Palacios A, Acedo A. From vineyard soil to wine fermentation: microbiome approximations to explain the “terroir” concept. Front Microbiol 2017; 8:821 [View Article] [PubMed]
     [Google Scholar]
  3. Kashif M, Jurvansuu J, Vainio EJ, Hantula J. Alphapartitiviruses of Heterobasidion wood decay fungi affect each other’s transmission and host growth. Front Cell Infect Microbiol 2019; 9: [View Article]
     [Google Scholar]
  4. Knowlton N, Rohwer F. Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 2003; 162:S51–S62 [View Article] [PubMed]
     [Google Scholar]
  5. Nerva L, Garcia JF, Favaretto F, Giudice G, Moffa L et al. The hidden world within plants: metatranscriptomics unveils the complexity of wood microbiomes. J Exp Bot 2022; 73:2682–2697 [View Article] [PubMed]
     [Google Scholar]
  6. Terhonen E, Blumenstein K, Kovalchuk A, Asiegbu FO. Forest tree microbiomes and associated fungal endophytes: functional roles and impact on forest health. Forests 2019; 10:42 [View Article]
     [Google Scholar]
  7. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A. The importance of the microbiome of the plant holobiont. New Phytol 2015; 206:1196–1206 [View Article] [PubMed]
     [Google Scholar]
  8. Pacifico D, Squartini A, Crucitti D, Barizza E, Lo Schiavo F et al. The role of the endophytic microbiome in the grapevine response to environmental triggers. Front Plant Sci 2019; 10: [View Article] [PubMed]
     [Google Scholar]
  9. Nuss DL. Biological control of chestnut blight: an example of virus-mediated attenuation of fungal pathogenesis. Microbiol Rev 1992; 56:561–576 [View Article] [PubMed]
     [Google Scholar]
  10. Rigling D, Prospero S. Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Mol Plant Pathol 2017; 19:7–20 [View Article] [PubMed]
     [Google Scholar]
  11. Zhang H, Xie J, Fu Y, Cheng J, Qu Z et al. A 2-kb mycovirus converts a pathogenic fungus into a beneficial endophyte for brassica protection and yield enhancement. Mol Plant 2020; 13:1420–1433 [View Article] [PubMed]
     [Google Scholar]
  12. Al Rwahnih M, Daubert S, Urbez-Torres JR, Cordero F, Rowhani A. Deep sequencing evidence from single grapevine plants reveals a virome dominated by mycoviruses. Arch Virol 2011; 156:397–403 [View Article] [PubMed]
     [Google Scholar]
  13. Chiapello M, Rodríguez-Romero J, Ayllón MA, Turina M. Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages. Virus Evol 2020; 6:veaa058 [View Article] [PubMed]
     [Google Scholar]
  14. Pandey B, Naidu RA, Grove GG. Detection and analysis of mycovirus-related RNA viruses from grape powdery mildew fungus Erysiphe necator. Arch Virol 2018; 163:1019–1030 [View Article] [PubMed]
     [Google Scholar]
  15. Bensch K, Groenewald JZ, Braun U, Dijksterhuis J, Starink M et al. Biodiversity in the cladosporium herbarum complex (davidiellaceae, capnodiales), with standardisation of methods for cladosporium taxonomy and diagnostics. Stud Mycol 2007; 58:105–156 [View Article] [PubMed]
     [Google Scholar]
  16. Deyett E, Rolshausen PE. Temporal dynamics of the sap microbiome of grapevine under high pierce’s disease pressure. Front Plant Sci 2019; 10:1246 [View Article] [PubMed]
     [Google Scholar]
  17. Nerva L, Turina M, Zanzotto A, Gardiman M, Gaiotti F et al. Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants. Environ Microbiol 2019; 21:2886–2904 [View Article] [PubMed]
     [Google Scholar]
  18. Liu D, Howell K. Community succession of the grapevine fungal microbiome in the annual growth cycle. Environ Microbiol 2021; 23:1842–1857 [View Article] [PubMed]
     [Google Scholar]
  19. Briceño EX, Latorre BA. Characterization of cladosporium rot in grapevines, a problem of growing importance in Chile. Plant Dis 2008; 92:1635–1642 [View Article] [PubMed]
     [Google Scholar]
  20. Hofstetter V, Buyck B, Croll D, Viret O, Couloux A et al. What if esca disease of grapevine were not a fungal disease?. Fungal Diversity 2012; 54:51–67 [View Article]
     [Google Scholar]
  21. Pilotti M, Faggioli F, Barba M. Characterization of italian isolates of pear vein yellows virus. In Acta Horticulturae Leuven, Belgium: International Society for Horticultural Science (ISHS); 1995 pp 148–154 [View Article]
     [Google Scholar]
  22. Mahillon M, Brodard J, Kellenberger I, Blouin AG, Schumpp O. A novel weevil-transmitted tymovirus found in mixed infection on hollyhock. Virol J 2023; 20:17 [View Article] [PubMed]
     [Google Scholar]
  23. Akbergenov R, Si-Ammour A, Blevins T, Amin I, Kutter C et al. Molecular characterization of geminivirus-derived small RNAs in different plant species. Nucleic Acids Res 2006; 34:462–471 [View Article] [PubMed]
     [Google Scholar]
  24. Candresse T, Filloux D, Muhire B, Julian C, Galzi S et al. Appearances can be deceptive: revealing a hidden viral infection with deep sequencing in a plant quarantine context. PLoS One 2014; 9:e102945 [View Article] [PubMed]
     [Google Scholar]
  25. Filloux D, Dallot S, Delaunay A, Galzi S, Jacquot E et al. Metagenomics approaches based on virion-associated nucleic acids (VANA): an innovative tool for assessing without a priori viral diversity of plants. In Lacomme C. ed Plant Pathology: Techniques and Protocols New York, NY: Springer; pp 249–257 [View Article]
     [Google Scholar]
  26. Maclot FJ, Debue V, Blouin AG, Fontdevila Pareta N, Tamisier L et al. Identification, molecular and biological characterization of two novel secovirids in wild grass species in Belgium. Virus Res 2021; 298:198397 [View Article] [PubMed]
     [Google Scholar]
  27. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  28. BBDuk Guide DOE Joint Genome Institute. n.d https://jgi.doe.gov/data-and-tools/software-tools/bbtools/bb-tools-user-guide/bbduk-guide/ accessed 5 June 2020
  29. Asamizu T, Summers D, Motika MB, Anzola JV, Nuss DL. Molecular cloning and characterization of the genome of wound tumor virus: a tumor-inducing plant reovirus. Virology 1985; 144:398–409 [View Article] [PubMed]
     [Google Scholar]
  30. Abràmoff DMD Image Processing with ImageJ; 2004Jul https://imagej.nih.gov/ij/docs/pdfs/Image_Processing_with_ImageJ.pdf
  31. Ahmed I, Li P, Zhang L, Jiang X, Bhattacharjee P et al. First report of a novel partitivirus from the phytopathogenic fungus fusarium cerealis in China. Arch Virol 2020; 165:2979–2983 [View Article] [PubMed]
     [Google Scholar]
  32. Nerva L, Silvestri A, Ciuffo M, Palmano S, Varese GC et al. Transmission of Penicillium aurantiogriseum partiti-like virus 1 to a new fungal host (Cryphonectria parasitica) confers higher resistance to salinity and reveals adaptive genomic changes. Environ Microbiol 2017; 19:4480–4492 [View Article] [PubMed]
     [Google Scholar]
  33. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
     [Google Scholar]
  34. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article] [PubMed]
     [Google Scholar]
  35. Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 2016; 44:W232–W235 [View Article] [PubMed]
     [Google Scholar]
  36. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2018; 35:518–522 [View Article] [PubMed]
     [Google Scholar]
  37. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B et al. Toward automatic reconstruction of a highly resolved tree of life. Science 2006; 311:1283–1287 [View Article] [PubMed]
     [Google Scholar]
  38. El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A et al. The pfam protein families database in 2019. Nucleic Acids Res 2019; 47:D427–D432 [View Article] [PubMed]
     [Google Scholar]
  39. Starr EP, Nuccio EE, Pett-Ridge J, Banfield JF, Firestone MK. Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil. Proc Natl Acad Sci 2019; 116:25900–25908 [View Article] [PubMed]
     [Google Scholar]
  40. Vainio EJ, Chiba S, Ghabrial SA, Maiss E, Roossinck M et al. ICTV virus taxonomy profile: partitiviridae. J Gen Virol 2018; 99:17–18 [View Article] [PubMed]
     [Google Scholar]
  41. Wang P, Yang G, Shi N, Zhao C, Hu F et al. A novel partitivirus orchestrates conidiation, stress response, pathogenicity, and secondary metabolism of the entomopathogenic fungus metarhizium majus. PLoS Pathog 2023; 19:e1011397 [View Article] [PubMed]
     [Google Scholar]
  42. Wang J, Youkharibache P, Zhang D, Lanczycki CJ, Geer RC et al. iCn3D, a web-based 3D viewer for sharing 1D/2D/3D representations of biomolecular structures. Bioinformatics 2020; 36:131–135 [View Article] [PubMed]
     [Google Scholar]
  43. Ochoa WF, Havens WM, Sinkovits RS, Nibert ML, Ghabrial SA et al. Partitivirus structure reveals a 120-subunit, helix-rich capsid with distinctive surface arches formed by quasisymmetric coat-protein dimers. Structure 2008; 16:776–786 [View Article] [PubMed]
     [Google Scholar]
  44. Chun J, Ko Y-H, Kim D-H. Transcriptome analysis of Cryphonectria parasitica infected with cryphonectria hypovirus 1 (CHV1) reveals distinct genes related to fungal metabolites, virulence, antiviral RNA-silencing, and their regulation. Front Microbiol 2020; 11:1711 [View Article] [PubMed]
     [Google Scholar]
  45. Lemus-Minor CG, Cañizares MC, García-Pedrajas MD, Pérez-Artés E. Fusarium oxysporum f. sp. dianthi virus 1 accumulation Is correlated with changes in virulence and other phenotypic traits of its fungal host. Phytopathology 2018; 108:957–963 [View Article] [PubMed]
     [Google Scholar]
  46. Xiao X, Cheng J, Tang J, Fu Y, Jiang D et al. A novel partitivirus that confers hypovirulence on plant pathogenic fungi. J Virol 2014; 88:10120–10133 [View Article] [PubMed]
     [Google Scholar]
  47. Ahn I-P, Lee Y-H. A viral double-stranded RNA up regulates the fungal virulence of Nectria radicicola. MPMI 2001; 14:496–507 [View Article] [PubMed]
     [Google Scholar]
  48. Bhatti MF, Jamal A, Petrou MA, Cairns TC, Bignell EM et al. The effects of dsRNA mycoviruses on growth and murine virulence of Aspergillus fumigatus. Fungal Genet Biol 2011; 48:1071–1075 [View Article] [PubMed]
     [Google Scholar]
  49. Filippou C, Diss RM, Daudu JO, Coutts RHA, Kotta-Loizou I. The polymycovirus-mediated growth enhancement of the entomopathogenic fungus Beauveria bassiana is dependent on carbon and nitrogen metabolism. Front Microbiol 2021; 12:606366 [View Article] [PubMed]
     [Google Scholar]
  50. Gilbert KB, Holcomb EE, Allscheid RL, Carrington JC. Hiding in plain sight: new virus genomes discovered via a systematic analysis of fungal public transcriptomes. PLoS One 2019; 14:e0219207 [View Article] [PubMed]
     [Google Scholar]
  51. Kamaruzzaman M, He G, Wu M, Zhang J, Yang L et al. A novel partitivirus in the hypovirulent isolate QT5-19 of the plant pathogenic fungus botrytis cinerea. Viruses 2019; 11:24 [View Article] [PubMed]
     [Google Scholar]
  52. Zheng L, Zhang M, Chen Q, Zhu M, Zhou E. A novel mycovirus closely related to viruses in the genus alphapartitivirus confers hypovirulence in the phytopathogenic fungus Rhizoctonia solani . Virology 2014; 456–457:220–226 [View Article] [PubMed]
     [Google Scholar]
  53. Latorre BA, Briceño EX, Torres R. Increase in cladosporium spp. populations and rot of wine grapes associated with leaf removal. Crop Protection 2011; 30:52–56 [View Article]
     [Google Scholar]
  54. McHale MT, Roberts IN, Noble SM, Beaumont C, Whitehead MP et al. CfT-I: an LTR-retrotransposon in cladosporium fulvum, a fungal pathogen of tomato. Mol Gen Genet 1992; 233:337–347 [View Article] [PubMed]
     [Google Scholar]
  55. Maheshwari R, Navaraj A. Senescence in fungi: the view from Neurospora. FEMS Microbiol Lett 2008; 280:135–143 [View Article] [PubMed]
     [Google Scholar]
  56. Maas MF, Debets AJ, Zwaan BJ. 17 why some fungi senesce and others do not. In The Evolution of Senescence in the Tree of Life vol 341 2017 [View Article]
     [Google Scholar]
  57. Vainio EJ, Jurvansuu J, Hyder R, Kashif M, Piri T et al. Heterobasidion partitivirus 13 mediates severe growth debilitation and major alterations in the gene expression of a fungal forest pathogen. J Virol 2018; 92:e01744-17 [View Article] [PubMed]
     [Google Scholar]
  58. Bozarth RF, Wood HA, Mandelbrot A. The Penicillium stoloniferum virus complex: two similar double-stranded RNA virus-like particles in a single cell. Virology 1971; 45:516–523 [View Article] [PubMed]
     [Google Scholar]
  59. Chiba S, Salaipeth L, Lin Y-H, Sasaki A, Kanematsu S et al. 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 2009; 83:12801–12812 [View Article] [PubMed]
     [Google Scholar]
  60. Wu M, Jin F, Zhang J, Yang L, Jiang D et al. Characterization of a novel bipartite double-stranded RNA mycovirus conferring hypovirulence in the phytopathogenic fungus botrytis porri. J Virol 2012; 86:6605–6619 [View Article] [PubMed]
     [Google Scholar]
  61. Liu L, Wang Q, Cheng J, Fu Y, Jiang D et al. Molecular characterization of a bipartite double-stranded RNA virus and its satellite-like RNA co-infecting the phytopathogenic fungus sclerotinia sclerotiorum. Front Microbiol 2015; 6:406 [View Article] [PubMed]
     [Google Scholar]
  62. Nibert ML, Ghabrial SA, Maiss E, Lesker T, Vainio EJ et al. Taxonomic reorganization of family partitiviridae and other recent progress in partitivirus research. Virus Res 2014; 188:128–141 [View Article] [PubMed]
     [Google Scholar]
  63. Wang Y, Zhao H, Cao J, Yin X, Guo Y et al. Characterization of a novel mycovirus from the phytopathogenic fungus Botryosphaeria dothidea. Viruses 2022; 14:331 [View Article] [PubMed]
     [Google Scholar]
  64. Hamim I, Urayama S-I, Netsu O, Tanaka A, Arie T et al. Discovery, genomic sequence characterization and phylogenetic analysis of novel RNA viruses in the turfgrass pathogenic Colletotrichum spp. in Japan. Viruses 2022; 14:2572 [View Article] [PubMed]
     [Google Scholar]
  65. Robertson JS. 5’ and 3’ terminal nucleotide sequences of the RNA genome segments of influenza virus. Nucleic Acids Res 1979; 6:3745–3757 [View Article] [PubMed]
     [Google Scholar]
  66. McDonald SM, Nelson MI, Turner PE, Patton JT. Reassortment in segmented RNA viruses: mechanisms and outcomes. Nat Rev Microbiol 2016; 14:448–460 [View Article] [PubMed]
     [Google Scholar]
  67. Gao Q, Palese P. Rewiring the RNAs of influenza virus to prevent reassortment. Proc Natl Acad Sci 2009; 106:15891–15896 [View Article] [PubMed]
     [Google Scholar]
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New viruses of Cladosporium sp. expand considerably the taxonomic structure of Gammapartitivirus genus
J. Gen. Virol. 104, 001879 (2023); https://doi.org/10.1099/jgv.0.001879
/content/journal/jgv/10.1099/jgv.0.001879
/content/journal/jgv/10.1099/jgv.0.001879
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