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Abstract

High-throughput virome analyses with various fungi, from cultured or uncultured sources, have led to the discovery of diverse viruses with unique genome structures and even neo-lifestyles. Examples in the former category include splipalmiviruses and ambiviruses. Splipalmiviruses, related to yeast narnaviruses, have multiple positive-sense (+) single-stranded (ss) RNA genomic segments that separately encode the RNA-dependent RNA polymerase motifs, the hallmark of RNA viruses (members of the kingdom ). Ambiviruses appear to have an undivided ssRNA genome of 3∼5 kb with two large open reading frames (ORFs) separated by intergenic regions. Another narna-like virus group has two fully overlapping ORFs on both strands of a genomic segment that span more than 90% of the genome size. New virus lifestyles exhibited by mycoviruses include the yado-kari/yado-nushi nature characterized by the partnership between the (+)ssRNA yadokarivirus and an unrelated dsRNA virus (donor of the capsid for the former) and the hadaka nature of capsidless 10–11 segmented (+)ssRNA accessible by RNase in infected mycelial homogenates. Furthermore, dsRNA polymycoviruses with phylogenetic affinity to (+)ssRNA animal caliciviruses have been shown to be infectious as dsRNA–protein complexes or deproteinized naked dsRNA. Many previous phylogenetic gaps have been filled by recently discovered fungal and other viruses, which haveprovided interesting evolutionary insights. Phylogenetic analyses and the discovery of natural and experimental cross-kingdom infections suggest that horizontal virus transfer may have occurred and continue to occur between fungi and other kingdoms.

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2022-08-26
2024-06-18
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Literature Cited

  1. 1.
    Abdoulaye AH, Hai D, Tang Q, Jiang D, Fu Y et al. 2021. Two distant helicases in one mycovirus: evidence of horizontal gene transfer between mycoviruses, coronaviruses and other nidoviruses. Virus Evol 7:veab043
    [Google Scholar]
  2. 2.
    Adams MJ, Adkins S, Bragard C, Gilmer D, Li D et al. 2017. ICTV virus taxonomy profile: Virgaviridae. J. Gen. Virol. 98:1999–2000
    [Google Scholar]
  3. 3.
    Ahn IP, Lee YH 2001. A viral double-stranded RNA up regulates the fungal virulence of Nectria radicicola. Mol. Plant-Microbe Interact. 14:496–507
    [Google Scholar]
  4. 4.
    Andika IB, Jamal A, Kondo H, Suzuki N. 2017. SAGA complex mediates the transcriptional up-regulation of antiviral RNA silencing. PNAS 114:E3499–E506
    [Google Scholar]
  5. 5.
    Andika IB, Kondo H, Suzuki N. 2019. Dicer functions transcriptionally and post-transcriptionally in a multilayer antiviral defense. PNAS 116:2274–81
    [Google Scholar]
  6. 6.
    Andika IB, Wei S, Cao C, Salaipeth L, Kondo H, Sun L. 2017. Phytopathogenic fungus hosts a plant virus: a naturally occurring cross-kingdom viral infection. PNAS 114:12267–72
    [Google Scholar]
  7. 7.
    Arjona-Lopez JM, Telengech P, Jamal A, Hisano S, Kondo H et al. 2018. Novel, diverse RNA viruses from Mediterranean isolates of the phytopathogenic fungus, Rosellinia necatrix: insights into evolutionary biology of fungal viruses. Environ. Microbiol. 20:1464–83
    [Google Scholar]
  8. 8.
    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
    [Google Scholar]
  9. 9.
    Aulia A, Hyodo K, Hisano S, Kondo H, Hillman BI, Suzuki N. 2021. Identification of an RNA silencing suppressor encoded by a symptomless fungal hypovirus, Cryphonectria hypovirus 4. Biology 10:100
    [Google Scholar]
  10. 10.
    Bejerman N, Debat H, Dietzgen RG. 2020. The plant negative-sense RNA virosphere: virus discovery through new eyes. Front. Microbiol. 11:588427
    [Google Scholar]
  11. 11.
    Bennett HM. 2014. Split reality for novel tick virus. Nat. Rev. Microbiol. 12:464
    [Google Scholar]
  12. 12.
    Bian R, Andika IB, Pang T, Lian Z, Wei S et al. 2020. Facilitative and synergistic interactions between fungal and plant viruses. PNAS 117:3779–88
    [Google Scholar]
  13. 13.
    Bock R. 2010. The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci 15:11–22
    [Google Scholar]
  14. 14.
    Botella L, Janousek J, Maia C, Jung MH, Raco M, Jung T 2020. Marine oomycetes of the genus Halophytophthora harbor viruses related to bunyaviruses. Front. Microbiol. 11:1467
    [Google Scholar]
  15. 15.
    Botella L, Jung T 2021. Multiple viral infections detected in Phytophthora condilina by total and small RNA sequencing. Viruses 13:620
    [Google Scholar]
  16. 16.
    Bruenn JA, Warner BE, Yerramsetty P 2015. Widespread narnavirus sequences in plant genomes. PeerJ 3:e876
    [Google Scholar]
  17. 17.
    Cai Q, He B, Wang S, Fletcher S, Niu D et al. 2021. Message in a bubble: shuttling small RNAs and proteins between cells and interacting organisms using extracellular vesicles. Annu. Rev. Plant Biol. 72:497–524
    [Google Scholar]
  18. 18.
    Canizares MC, Lopez-Escudero FJ, Perez-Artes E, Garcia-Pedrajas MD. 2018. Characterization of a novel single-stranded RNA mycovirus related to invertebrate viruses from the plant pathogen Verticillium dahliae. Arch. Virol. 163:771–76
    [Google Scholar]
  19. 19.
    Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–73
    [Google Scholar]
  20. 20.
    Chabi-Jesus C, Najar A, Fontenele RS, Kumari SG, Ramos-Gonzalez PL et al. 2020. Viruses representing two new genomovirus species identified in citrus from Tunisia. Arch. Virol. 165:1225–29
    [Google Scholar]
  21. 21.
    Charon J, Grigg MJ, Eden JS, Piera KA, Rana H et al. 2019. Novel RNA viruses associated with Plasmodium vivax in human malaria and Leucocytozoon parasites in avian disease. PLOS Pathog 15:e1008216
    [Google Scholar]
  22. 22.
    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
    [Google Scholar]
  23. 23.
    Chiba S, Kondo H, Tani A, Saisho D, Sakamoto W et al. 2011. Widespread endogenization of genome sequences of non-retroviral RNA viruses into plant genomes. PLOS Pathog 7:e1002146
    [Google Scholar]
  24. 24.
    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. 83:12801–12
    [Google Scholar]
  25. 25.
    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
    [Google Scholar]
  26. 26.
    Chiba Y, Oiki S, Zhao Y, Nagano Y, Urayama SI, Hagiwara D. 2021. Splitting of RNA-dependent RNA polymerase is common in Narnaviridae: identification of a type II divided RdRp from deep-sea fungal isolates. Virus Evol 7:veab095
    [Google Scholar]
  27. 27.
    Cho WK, Lee KM, Yu J, Son M, Kim KH 2013. Insight into mycoviruses infecting Fusarium species. Adv. Virus Res. 86:273–88
    [Google Scholar]
  28. 28.
    Das S, Alam MM, Zhang R, Hisano S, Suzuki N. 2021. Proof of concept of the yadokari nature: a capsidless replicase-encoding but replication-dependent positive-sense single-stranded RNA virus hosted by an unrelated double-stranded RNA virus. J. Virol. 95:e0046721
    [Google Scholar]
  29. 29.
    Deakin G, Dobbs E, Bennett JM, Jones IM, Grogan HM, Burton KS. 2017. Multiple viral infections in Agaricus bisporus: characterisation of 18 unique RNA viruses and 8 ORFans identified by deep sequencing. Sci. Rep 7:12469
    [Google Scholar]
  30. 30.
    Degola F, Spadola G, Forgia M, Turina M, Dramis L et al. 2021. Aspergillus goes viral: ecological insights from the geographical distribution of the mycovirome within an Aspergillus flavus population and its possible correlation with aflatoxin biosynthesis. J. Fungi 7:10833
    [Google Scholar]
  31. 31.
    DeRisi JL, Huber G, Kistler A, Retallack H, Wilkinson M, Yllanes D. 2019. An exploration of ambigrammatic sequences in narnaviruses. Sci. Rep. 9:17982
    [Google Scholar]
  32. 32.
    Dietzgen RG, Kondo H, Goodin MM, Kurath G, Vasilakis N. 2017. The family Rhabdoviridae: mono- and bipartite negative-sense RNA viruses with diverse genome organization and common evolutionary origins. Virus Res 227:158–70
    [Google Scholar]
  33. 33.
    Dinan AM, Lukhovitskaya NI, Olendraite I, Firth AE. 2020. A case for a negative-strand coding sequence in a group of positive-sense RNA viruses. Virus Evol 6:veaa007
    [Google Scholar]
  34. 34.
    Dolja VV, Koonin EV. 2018. Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer. Virus Res 244:36–52
    [Google Scholar]
  35. 35.
    Dolja VV, Krupovic M, Koonin EV. 2020. Deep roots and splendid boughs of the global plant virome. Annu. Rev. Phytopathol. 58:23–53
    [Google Scholar]
  36. 36.
    Donaire L, Ayllon MA. 2017. Deep sequencing of mycovirus-derived small RNAs from Botrytis species. Mol. Plant Pathol. 18:1127–37
    [Google Scholar]
  37. 37.
    Donaire L, Pagan I, Ayllon 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 499:212–18
    [Google Scholar]
  38. 38.
    Donaire L, Rozas J, Ayllon MA. 2016. Molecular characterization of Botrytis ourmia-like virus, a mycovirus close to the plant pathogenic genus Ourmiavirus. Virology 489:158–64
    [Google Scholar]
  39. 39.
    Esteban R, Vega L, Fujimura T. 2008. 20S RNA narnavirus defies the antiviral activity of SKI1/XRN1 in Saccharomyces cerevisiae. J. Biol. Chem. 283:25812–20
    [Google Scholar]
  40. 40.
    Feng C, Feng J, Wang Z, Pedersen C, Wang X 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:e0026421
    [Google Scholar]
  41. 41.
    Flores R, Navarro B, Sera P, Di Serio F. 2022. A scenario for the emergence of protoviroids in the RNA world and for their further evolution into viroids and viroid-like RNAs by modular recombinations and mutations. Virus Evol 8:veab107
    [Google Scholar]
  42. 42.
    Forgia M, Isgandarli E, Aghayeva DN, Huseynova I, Turina M. 2021. Virome characterization of Cryphonectria parasitica isolates from Azerbaijan unveiled a new mymonavirus and a putative new RNA virus unrelated to described viral sequences. Virology 553:51–61
    [Google Scholar]
  43. 43.
    Fujimura T, Esteban R 2004. The bipartite 3′-cis-acting signal for replication is required for formation of a ribonucleoprotein complex in vivo between the viral genome and its RNA polymerase in yeast 23 S RNA virus. J. Biol. Chem. 279:44219–28
    [Google Scholar]
  44. 44.
    Fujimura T, Esteban R 2007. Interactions of the RNA polymerase with the viral genome at the 5′- and 3′-ends contribute to 20S RNA narnavirus persistence in yeast. J. Biol. Chem. 282:19011–19
    [Google Scholar]
  45. 45.
    Fujimura T, Solorzano A, Esteban R 2005. Native replication intermediates of the yeast 20 S RNA virus have a single-stranded RNA backbone. J. Biol. Chem. 280:7398–406
    [Google Scholar]
  46. 46.
    Fukushi T. 1969. Relationships between propagative rice viruses and their vectors. Viruses, Vectors, and Vegetation K Maramorosch 279–301 New York: Wiley
    [Google Scholar]
  47. 47.
    Garcia ML, Dal Bo E, da Graca JV, Gago-Zachert S, Hammond J et al. 2017. ICTV virus taxonomy profile: Ophioviridae. J. Gen. Virol. 98:1161–62
    [Google Scholar]
  48. 48.
    Garcia-Pedrajas MD, Canizares MC, Sarmiento-Villamil JL, Jacquat AG, Dambolena JS. 2019. Mycoviruses in biological control: from basic research to field implementation. Phytopathology 109:1828–39
    [Google Scholar]
  49. 49.
    German TL, Lorenzen MD, Grubbs N, Whitfield AE. 2020. New technologies for studying negative-strand RNA viruses in plant and arthropod hosts. Mol. Plant-Microbe Interact. 33:382–93
    [Google Scholar]
  50. 50.
    Ghabrial SA, Caston JR, Jiang D, Nibert ML, Suzuki N. 2015. 50-plus years of fungal viruses. Virology 479–480:356–68
    [Google Scholar]
  51. 51.
    Ghabrial SA, Suzuki N. 2009. Viruses of plant pathogenic fungi. Annu. Rev. Phytopathol. 47:353–84
    [Google Scholar]
  52. 52.
    Gilbert KB, Holcomb EE, Allscheid RL, Carrington JC. 2019. Hiding in plain sight: new virus genomes discovered via a systematic analysis of fungal public transcriptomes. PLOS ONE 14:e0219207
    [Google Scholar]
  53. 53.
    Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307–21
    [Google Scholar]
  54. 54.
    Hansen DR, Vanalfen NK, Gillies K, Powell WA. 1985. Naked dsRNA associated with hypovirulence of Endothia parasitica is packaged in fungal vesicles. J. Gen. Virol. 66:2605–14
    [Google Scholar]
  55. 55.
    Hao F, Wu M, Li G. 2021. Characterization of a novel genomovirus in the phytopathogenic fungus Botrytis cinerea. Virology 553:111–16
    [Google Scholar]
  56. 56.
    He B, Cai Q, Qiao L, Huang CY, Wang S et al. 2021. RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles. Nat. Plants 7:342–52
    [Google Scholar]
  57. 57.
    Hillman BI, Aulia A, Suzuki N. 2018. Viruses of plant-interacting fungi. Adv. Virus Res. 100:99–116
    [Google Scholar]
  58. 58.
    Hillman BI, Suzuki N. 2004. Viruses of the chestnut blight fungus, Cryphonectria parasitica. Adv. Virus Res. 63:423–72
    [Google Scholar]
  59. 59.
    Hisano S, Zhang R, Faruk MI, Kondo H, Suzuki N. 2018. A neo-virus lifestyle exhibited by a (+)ssRNA virus hosted in an unrelated dsRNA virus: taxonomic and evolutionary considerations. Virus Res 244:75–83
    [Google Scholar]
  60. 60.
    Honda S, Eusebio-Cope A, Miyashita S, Yokoyama A, Aulia A et al. 2020. Establishment of Neurospora crassa as a model organism for fungal virology. Nat. Commun. 11:5627
    [Google Scholar]
  61. 61.
    Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T et al. 2010. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463:84–87
    [Google Scholar]
  62. 62.
    Jia H, Dong K, Zhou L, Wang G, Hong N et al. 2017. A dsRNA virus with filamentous viral particles. Nat. Commun. 8:168
    [Google Scholar]
  63. 63.
    Jia J, Fu Y, Jiang D, Mu F, Cheng J et al. 2021. Interannual dynamics, diversity and evolution of the virome in Sclerotinia sclerotiorum from a single crop field. Virus Evol 7:veab032
    [Google Scholar]
  64. 64.
    Kanhayuwa L, Kotta-Loizou I, Ozkan S, Gunning AP, Coutts RH. 2015. A novel mycovirus from Aspergillus fumigatus contains four unique dsRNAs as its genome and is infectious as dsRNA. PNAS 112:9100–5
    [Google Scholar]
  65. 65.
    Katoh K, Rozewicki J, Yamada KD. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 20:1160–66
    [Google Scholar]
  66. 66.
    Katzourakis A, Gifford RJ. 2010. Endogenous viral elements in animal genomes. PLOS Genet 6:11e1001191
    [Google Scholar]
  67. 67.
    Kawasaki J, Kojima S, Mukai Y, Tomonaga K, Horie M. 2021. 100-My history of bornavirus infections hidden in vertebrate genomes. PNAS 118:20e2026235118
    [Google Scholar]
  68. 68.
    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. 166:2711–22
    [Google Scholar]
  69. 69.
    Khan HA, Shamsi W, Jamal A, Javaied M, Sadiq M et al. 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. https://doi.org/10.1099/jgv.0.001690
    [Crossref] [Google Scholar]
  70. 70.
    Kondo H, Chiba S, Maruyama K, Andika IB, Suzuki N. 2019. A novel insect-infecting virga/nege-like virus group and its pervasive endogenization into insect genomes. Virus Res 262:37–47
    [Google Scholar]
  71. 71.
    Kondo H, Chiba S, Suzuki N. 2015. Detection and analysis of non-retroviral RNA virus-like elements in plant, fungal, and insect genomes. Methods Mol. Biol. 1236:73–88
    [Google Scholar]
  72. 72.
    Kondo H, Chiba S, Toyoda K, Suzuki N. 2013. Evidence for negative-strand RNA virus infection in fungi. Virology 435:201–9
    [Google Scholar]
  73. 73.
    Kondo H, Hirota K, Maruyama K, An'dika IB, Suzuki N 2017. A possible occurrence of genome reassortment among bipartite rhabdoviruses. Virology 508:18–25
    [Google Scholar]
  74. 74.
    Kondo H, Kanematsu S, Suzuki N. 2013. Viruses of the white root rot fungus, Rosellinia necatrix. Adv. Virus Res. 86:177–214
    [Google Scholar]
  75. 75.
    Koonin EV, Dolja VV, Krupovic M. 2015. Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479–480:2–25
    [Google Scholar]
  76. 76.
    Kormelink R, Garcia ML, Goodin M, Sasaya T, Haenni AL. 2011. Negative-strand RNA viruses: the plant-infecting counterparts. Virus Res 162:184–202
    [Google Scholar]
  77. 77.
    Kotta-Loizou I. 2021. Mycoviruses and their role in fungal pathogenesis. Curr. Opin. Microbiol. 63:10–18
    [Google Scholar]
  78. 78.
    Kotta-Loizou I, Coutts RHA. 2017. Studies on the virome of the entomopathogenic fungus Beauveria bassiana reveal novel dsRNA elements and mild hypervirulence. PLOS Pathog 13:e1006183
    [Google Scholar]
  79. 79.
    Kraberger S, Cook CN, Schmidlin K, Fontenele RS, Bautista J et al. 2019. Diverse single-stranded DNA viruses associated with honey bees (Apis mellifera). Infect. Genet. Evol. 71:179–88
    [Google Scholar]
  80. 80.
    Kraberger S, Schmidlin K, Fontenele RS, Walters M, Varsani A. 2019. Unravelling the single-stranded DNA virome of the New Zealand blackfly. Viruses 11:6532
    [Google Scholar]
  81. 81.
    Lefeuvre P, Martin DP, Elena SF, Shepherd DN, Roumagnac P, Varsani A. 2019. Evolution and ecology of plant viruses. Nat. Rev. Microbiol. 17:632–44
    [Google Scholar]
  82. 82.
    Li P, Bhattacharjee P, Wang S, Zhang L, Ahmed I, Guo L 2019. Mycoviruses in Fusarium species: an update. Front. Cell. Infect. Microbiol. 9:257
    [Google Scholar]
  83. 83.
    Li PF, Wang SC, Zhang LH, Qiu DW, Zhou XP, Guo LH. 2020. A tripartite ssDNA mycovirus from a plant pathogenic fungus is infectious as cloned DNA and purified virions. Sci. Adv. 6:eaay9634
    [Google Scholar]
  84. 84.
    Lin YH, Fujita M, Chiba S, Hyodo K, Andika IB et al. 2019. Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes). Virology 533:125–36
    [Google Scholar]
  85. 85.
    Linnakoski R, Sutela S, Coetzee MPA, Duong TA, Pavlov IN et al. 2021. Armillaria root rot fungi host single-stranded RNA viruses. Sci. Rep. 11:7336
    [Google Scholar]
  86. 86.
    Liu H, Fu Y, Jiang D, Li G, Xie J et al. 2010. Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J. Virol. 84:11876–87
    [Google Scholar]
  87. 87.
    Liu H, Fu Y, Xie J, Cheng J, Ghabrial SA et al. 2012. Evolutionary genomics of mycovirus-related dsRNA viruses reveals cross-family horizontal gene transfer and evolution of diverse viral lineages. BMC Evol. Biol. 12:91
    [Google Scholar]
  88. 88.
    Liu H, Wang H, Lu X, Xiao C, Peng B, Zhou Q. 2021. Molecular characterization of a novel single-stranded RNA virus, ChRV1, isolated from the plant-pathogenic fungus Colletotrichum higginsianum. Arch. Virol. 166:1805–9
    [Google Scholar]
  89. 89.
    Liu L, Xie J, Cheng J, Fu Y, Li G et al. 2014. Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses. PNAS 111:12205–10
    [Google Scholar]
  90. 90.
    Liu S, Xie JT, Cheng JS, Li B, Chen T et al. 2016. Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector. PNAS 113:12803–8
    [Google Scholar]
  91. 91.
    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
    [Google Scholar]
  92. 92.
    Marzano SYL, Domier LL. 2016. Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res 213:332–42
    [Google Scholar]
  93. 93.
    Marzano SYL, Nelson BD, Ajayi-Oyetunde O, Bradley CA, Hughes TJ et al. 2016. Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J. Virol. 90:6846–63
    [Google Scholar]
  94. 94.
    Mascia T, Nigro F, Abdallah A, Ferrara M, De Stradis A et al. 2014. Gene silencing and gene expression in phytopathogenic fungi using a plant virus vector. PNAS 111:4291–96
    [Google Scholar]
  95. 95.
    Mizutani Y, Abraham A, Uesaka K, Kondo H, Suga H et al. 2018. Novel mitoviruses and a unique tymo-like virus in hypovirulent and virulent strains of the Fusarium head bight fungus, Fusarium boothii. Viruses 10:584
    [Google Scholar]
  96. 96.
    Moleleki N, van Heerden SW, Wingfield MJ, Wingfield BD, Preisig O. 2003. Transfection of Diaporthe perjuncta with Diaporthe RNA virus. Appl. Environ. Microbiol. 69:3952–56
    [Google Scholar]
  97. 97.
    Morris TJ, Dodds JA. 1979. Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–58
    [Google Scholar]
  98. 98.
    Mu F, Li B, Cheng SF, Jia JC, Jiang DH et al. 2021. Nine viruses from eight lineages exhibiting new evolutionary modes that co-infect a hypovirulent phytopathogenic fungus. PLOS Pathog 17:e1009823
    [Google Scholar]
  99. 99.
    Mu F, Xie J, Cheng S, You MP, Barbetti MJ et al. 2017. Virome characterization of a collection of S. sclerotiorum from Australia. Front. Microbiol. 8:2540
    [Google Scholar]
  100. 100.
    Munoz-Adalia EJ, Diez JJ, Fernandez MM, Hantula J, Vainio EJ. 2018. Characterization of small RNAs originating from mitoviruses infecting the conifer pathogen Fusarium circinatum. Arch. Virol. 163:1009–18
    [Google Scholar]
  101. 101.
    Myers JM, Bonds AE, Clemons RA, Thapa NA, Simmons DR et al. 2020. Survey of early-diverging lineages of fungi reveals abundant and diverse mycoviruses. mBio 11:e02027–20
    [Google Scholar]
  102. 102.
    Navarro B, Minutolo M, De Stradis A, Palmisano F, Alioto D, Di Serio F. 2018. The first phlebo-like virus infecting plants: a case study on the adaptation of negative-stranded RNA viruses to new hosts. Mol. Plant Pathol. 19:1075–89
    [Google Scholar]
  103. 103.
    Nerva L, Ciuffo M, Vallino M, Margaria P, Varese GC et al. 2016. Multiple approaches for the detection and characterization of viral and plasmid symbionts from a collection of marine fungi. Virus Res 219:22–38
    [Google Scholar]
  104. 104.
    Nerva L, Forgia M, Ciuffo M, Chitarra W, Chiapello M et al. 2019. The mycovirome of a fungal collection from the sea cucumber Holothuria polii. Virus Res 273:197737
    [Google Scholar]
  105. 105.
    Nerva L, Turina M, Zanzotto A, Gardiman M, Gaiotti F et al. 2019. Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants. Environ. Microbiol. 21:2886–904
    [Google Scholar]
  106. 106.
    Nerva L, Varese GC, Falk BW, Turina M. 2017. Mycoviruses of an endophytic fungus can replicate in plant cells: evolutionary implications. Sci. Rep. 7:1908
    [Google Scholar]
  107. 107.
    Nerva L, Vigani G, Di Silvestre D, Ciuffo M, Forgia M et al. 2019. Biological and molecular characterization of Chenopodium quinoa mitovirus 1 reveals a distinct small RNA response compared to those of cytoplasmic RNA viruses. J. Virol. 93:e01998–18
    [Google Scholar]
  108. 108.
    Ng TF, Chen LF, Zhou Y, Shapiro B, Stiller M et al. 2014. Preservation of viral genomes in 700-y-old caribou feces from a subarctic ice patch. PNAS 111:16842–47
    [Google Scholar]
  109. 109.
    Nibert ML, Vong M, Fugate KK, Debat HJ. 2018. Evidence for contemporary plant mitoviruses. Virology 518:14–24
    [Google Scholar]
  110. 110.
    Nuss DL. 1992. Biological control of chestnut blight: an example of virus-mediated attenuation of fungal pathogenesis. Microbiol. Rev. 56:561–76
    [Google Scholar]
  111. 111.
    Nuss DL. 2011. Mycoviruses, RNA silencing, and viral RNA recombination. Adv. Virus Res. 80:25–48
    [Google Scholar]
  112. 112.
    Ojosnegros S, Garcia-Arriaza J, Escarmis C, Manrubia SC, Perales C et al. 2011. Viral genome segmentation can result from a trade-off between genetic content and particle stability. PLOS Genet 7:e1001344
    [Google Scholar]
  113. 113.
    Okada R, Ichinose S, Takeshita K, Urayama SI, Fukuhara T et al. 2018. Molecular characterization of a novel mycovirus in Alternaria alternata manifesting two-sided effects: down-regulation of host growth and up-regulation of host plant pathogenicity. Virology 519:23–32
    [Google Scholar]
  114. 114.
    Osaki H, Sasaki A, Nomiyama K, Tomioka K. 2016. Multiple virus infection in a single strain of Fusarium poae shown by deep sequencing. Virus Genes 52:835–47
    [Google Scholar]
  115. 115.
    Owashi Y, Aihara M, Moriyama H, Arie T, Teraoka T, Komatsu K 2020. Population structure of double-stranded RNA mycoviruses that infect the rice blast fungus Magnaporthe oryzae in Japan. Front. Microbiol. 11:593784
    [Google Scholar]
  116. 116.
    Ozkan S, Coutts RHA 2015. Aspergillus fumigatus mycovirus causes mild hypervirulent effect on pathogenicity when tested on Galleria mellonella. Fungal Genet. Biol 76:20–26
    [Google Scholar]
  117. 117.
    Pearson MN, Bailey AM. 2013. Viruses of Botrytis. Adv. Virus Res. 86:249–72
    [Google Scholar]
  118. 118.
    Picarelli M, Forgia M, Rivas EB, Nerva L, Chiapello M et al. 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
    [Google Scholar]
  119. 119.
    Polashock JJ, Hillman BI. 1994. A small mitochondrial double-stranded (ds) RNA element associated with a hypovirulent strain of the chestnut blight fungus and ancestrally related to yeast cytoplasmic T and W dsRNAs. PNAS 91:8680–84
    [Google Scholar]
  120. 120.
    Preisig O, Moleleki N, Smit WA, Wingfield BD, Wingfield MJ. 2000. A novel RNA mycovirus in a hypovirulent isolate of the plant pathogen Diaporthe ambigua. J. Gen. Virol. 81:3107–14
    [Google Scholar]
  121. 121.
    Pu Y, Kikuchi A, Moriyasu Y, Tomaru M, Jin Y et al. 2011. Rice dwarf viruses with dysfunctional genomes generated in plants are filtered out in vector insects: implications for the origin of the virus. J. Virol. 85:2975–79
    [Google Scholar]
  122. 122.
    Qu Z, Zhang H, Wang Q, Zhao H, Liu X et al. 2021. Exploring the symbiotic mechanism of a virus-mediated endophytic fungus in its host by dual unique molecular identifier-RNA sequencing. mSystems 6:e0081421
    [Google Scholar]
  123. 123.
    Ramirez BC, Haenni AL. 2021. Tenuiviruses (Phenuiviridae). Encyclopedia of Virology D Bamford, M Zuckerman 719–26 Oxford, UK: Elsevier. , 4th ed..
    [Google Scholar]
  124. 124.
    Rastgou M, Habibi MK, Izadpanah K, Masenga V, Milne RG et al. 2009. Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin. J. Gen. Virol. 90:2525–35
    [Google Scholar]
  125. 125.
    Resende RO, Pappu H. 2021. Orthotospoviruses (Tospoviridae). Encyclopedia of Virology D Bamford, M Zuckerman 5057–515 Oxford: Elsevier. , 4th ed..
    [Google Scholar]
  126. 126.
    Retallack H, Popova KD, Laurie MT, Sunshine S, DeRisi JL 2021. Persistence of ambigrammatic narnaviruses requires translation of the reverse open reading frame. J. Virol. 95:13e0010921
    [Google Scholar]
  127. 127.
    Rigling D, Prospero S. 2018. Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Mol. Plant Pathol. 19:7–20
    [Google Scholar]
  128. 128.
    Rodriguez-Cousino N, Esteban LM, Esteban R 1991. Molecular cloning and characterization of W double-stranded RNA, a linear molecule present in Saccharomyces cerevisiae. Identification of its single-stranded RNA form as 20 S RNA. J. Biol. Chem. 266:12772–78
    [Google Scholar]
  129. 129.
    Roossinck MJ. 2019. Evolutionary and ecological links between plant and fungal viruses. New Phytol 221:86–92
    [Google Scholar]
  130. 130.
    Rott ME, Kesanakurti P, Berwarth C, Rast H, Boyes I et al. 2018. Discovery of negative-sense RNA viruses in trees infected with apple rubbery wood disease by next-generation sequencing. Plant Dis 102:1254–63
    [Google Scholar]
  131. 131.
    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:e03705–20
    [Google Scholar]
  132. 132.
    Sa Antunes TF, Amaral RJ, Ventura JA, Godinho MT, Amaral JG et al. 2016. The dsRNA virus Papaya meleira virus and an ssRNA virus are associated with papaya sticky disease. PLOS ONE 11:e0155240
    [Google Scholar]
  133. 133.
    Sasai S, Tamura K, Tojo M, Herrero ML, Hoshino T et al. 2018. A novel non-segmented double-stranded RNA virus from an Arctic isolate of Pythium polare. Virology 522:234–43
    [Google Scholar]
  134. 134.
    Sato Y, Jamal A, Kondo H, Suzuki N. 2020. Molecular characterization of a novel polymycovirus from Penicillium janthinellum with a focus on its genome-associated PASrp. Front. Microbiol. 11:592789
    [Google Scholar]
  135. 135.
    Sato Y, Shahi S, Telengech P, Hisano S, Cornejo C et al. 2022. A new tetra-segmented splipalmivirus with divided RdRP domains from Cryphonectria naterciae, a fungus found on chestnut and cork oak trees in Europe. Virus Res 307:198606
    [Google Scholar]
  136. 136.
    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:e00450–20
    [Google Scholar]
  137. 137.
    Segers GC, van Wezel R, Zhang X, Hong Y, Nuss DL. 2006. Hypovirus papain-like protease p29 suppresses RNA silencing in the natural fungal host and in a heterologous plant system. Eukaryot. Cell 5:896–904
    [Google Scholar]
  138. 138.
    Segers GC, Zhang X, Deng F, Sun Q, Nuss DL. 2007. Evidence that RNA silencing functions as an antiviral defense mechanism in fungi. PNAS 104:12902–6
    [Google Scholar]
  139. 139.
    Shah UA, Kotta-Loizou I, Fitt BDL, Coutts RHA. 2020. Mycovirus-induced hypervirulence of Leptosphaeria biglobosa enhances systemic acquired resistance to Leptosphaeria maculans in Brassica napus. Mol. Plant-Microbe Interact. 33:98–107
    [Google Scholar]
  140. 140.
    Shi M, Lin XD, Chen X, Tian JH, Chen LJ et al. 2018. The evolutionary history of vertebrate RNA viruses. Nature 556:197–202
    [Google Scholar]
  141. 141.
    Shi M, Lin XD, Tian JH, Chen LJ, Chen X et al. 2016. Redefining the invertebrate RNA virosphere. Nature 540:539–43
    [Google Scholar]
  142. 142.
    Shi M, Lin XD, Vasilakis N, Tian JH, Li CX et al. 2016. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J. Virol. 90:659–69
    [Google Scholar]
  143. 143.
    Siddell SG, Walker PJ, Lefkowitz EJ, Mushegian AR, Adams MJ et al. 2019. Additional changes to taxonomy ratified in a special vote by the International Committee on Taxonomy of Viruses; October 2018. Arch. Virol. 164:943–46
    [Google Scholar]
  144. 144.
    Siddell SG, Walker PJ, Lefkowitz EJ, Mushegian AR, Dutilh BE et al. 2020. Binomial nomenclature for virus species: a consultation. Arch. Virol. 165:51925Correction 2020. Arch. Virol 165:126364
    [Google Scholar]
  145. 145.
    Silvestri A, Turina M, Fiorilli V, Miozzi L, Venice F et al. 2020. Different genetic sources contribute to the small RNA population in the arbuscular mycorrhizal fungus Gigaspora margarita. Front. Microbiol. 11:395
    [Google Scholar]
  146. 146.
    Smith K, Fielding R, Schiavone K, Hall KR, Reid VS et al. 2021. Circular DNA viruses identified in short-finned pilot whale and orca tissue samples. Virology 559:156–64
    [Google Scholar]
  147. 147.
    Solorzano A, Rodriguez-Cousino N, Esteban R, Fujimura T 2000. Persistent yeast single-stranded RNA viruses exist in vivo as genomic RNA center dot RNA polymerase complexes in 1:1 stoichiometry. J. Biol. Chem. 275:26428–35
    [Google Scholar]
  148. 148.
    Sun L, Kondo H, Andika IB. 2021. Cross-kingdom virus infection. Encyclopedia of Virology D Bamford, M Zuckerman 443–49 Oxford, UK: Elsevier. , 4th ed..
    [Google Scholar]
  149. 149.
    Sutela S, Forgia M, Vainio EJ, Chiapello M, Daghino S et al. 2020. The virome from a collection of endomycorrhizal fungi reveals new viral taxa with unprecedented genome organization. Virus Evol 6:veaa076
    [Google Scholar]
  150. 150.
    Sutela S, Piri T, Vainio EJ. 2021. Discovery and community dynamics of novel ssRNA mycoviruses in the conifer pathogen Heterobasidion parviporum. Front. Microbiol. 12:770787
    [Google Scholar]
  151. 151.
    Sutela S, Poimala A, Vainio EJ. 2019. Viruses of fungi and oomycetes in the soil environment. FEMS Microbiol. Ecol. 95:fiz119
    [Google Scholar]
  152. 152.
    Suzuki N. 2021. An introduction to fungal viruses. Encyclopedia of Virology D Bamford, M Zuckerman 431–42 Oxford: Elsevier. , 4th ed..
    [Google Scholar]
  153. 153.
    Suzuki N, Ghabrial SA, Kim KH, Pearson M, Marzano SL et al. 2018. ICTV virus taxonomy profile: Hypoviridae. J. Gen. Virol. 99:615–16
    [Google Scholar]
  154. 154.
    Takahashi H, Fukuhara T, Kitazawa H, Kormelink R. 2019. Virus latency and the impact on plants. Front. Microbiol 10:2764
    [Google Scholar]
  155. 155.
    Tamada T, Kondo H. 2013. Biological and genetic diversity of plasmodiophorid-transmitted viruses and their vectors. J. Gen. Plant Pathol. 79:307–20
    [Google Scholar]
  156. 156.
    ter Horst AM, Nigg JC, Dekker FM, Falk BW. 2019. Endogenous viral elements are widespread in arthropod genomes and commonly give rise to PIWI-interacting RNAs. J. Virol. 93:6e02124–18
    [Google Scholar]
  157. 157.
    Turina M, Ghignone S, Astolfi N, Silvestri A, Bonfante P, Lanfranco L. 2018. The virome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals the first report of DNA fragments corresponding to replicating non-retroviral RNA viruses in fungi. Environ. Microbiol. 20:62012–25
    [Google Scholar]
  158. 158.
    Urayama SI, Takaki Y, Nishi S, Yoshida-Takashima Y, Deguchi S et al. 2018. Unveiling the RNA virosphere associated with marine microorganisms. Mol. Ecol. Resour. 18:1444–55
    [Google Scholar]
  159. 159.
    Urayama SI, Takaki Y, Nunoura T. 2016. FLDS: a comprehensive dsRNA sequencing method for intracellular RNA virus surveillance. Microbes Environ 31:33–40
    [Google Scholar]
  160. 160.
    Vainio EJ. 2019. Mitoviruses in the conifer root rot pathogens Heterobasidion annosum and H. parviporum. Virus Res 271:197681
    [Google Scholar]
  161. 161.
    Vainio EJ, Jurvansuu J, Hyder R, Kashif M, Piri T et al. 2018. Heterobasidion partitivirus 13 mediates severe growth debilitation and major alterations in the gene expression of a fungal forest pathogen. J. Virol. 92:e01744–17
    [Google Scholar]
  162. 162.
    Valverde RA, Khalifa ME, Okada R, Fukuhara T, Sabanadzovic S, ICTV Rep. Consort. 2019. ICTV virus taxonomy profile: Endornaviridae. J. Gen. Virol. 100:1204–5
    [Google Scholar]
  163. 163.
    Varsani A, Krupovic M. 2021. Family Genomoviridae: 2021 taxonomy update. Arch. Virol. 166:2911–26
    [Google Scholar]
  164. 164.
    Velasco L, Arjona-Girona I, Cretazzo E, Lopez-Herrera C. 2019. Viromes in Xylariaceae fungi infecting avocado in Spain. Virology 532:11–21
    [Google Scholar]
  165. 165.
    Vong M, Manny AR, Smith KL, Gao W, Nibert ML. 2019. Beta vulgaris mitovirus 1 in diverse cultivars of beet and chard. Virus Res 265:80–87
    [Google Scholar]
  166. 166.
    Wagemans J, Holtappels D, Vainio E, Rabiey M, Marzachi C et al. 2022. Going viral: virus-based biological control agents for plant protection. Annu. Rev. Phytopathol. 60:2142
    [Google Scholar]
  167. 167.
    Walker PJ, Blasdell KR, Calisher CH, Dietzgen RG, Kondo H et al. 2018. ICTV virus taxonomy profile: Rhabdoviridae. J. Gen. Virol. 99:447–48
    [Google Scholar]
  168. 168.
    Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Dempsey DM et al. 2019. Changes to virus taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses 2019. Arch. Virol. 164:2417–29
    [Google Scholar]
  169. 169.
    Wang J, Ni YX, Liu XT, Zhao H, Xiao YN et al. 2021. Divergent RNA viruses in Macrophomina phaseolina exhibit potential as virocontrol agents. Virus Evol 7:veaa095
    [Google Scholar]
  170. 170.
    Wang L, He H, Wang S, Chen X, Qiu D et al. 2018. Evidence for a novel negative-stranded RNA mycovirus isolated from the plant pathogenic fungus Fusarium graminearum. Virology 518:232–40
    [Google Scholar]
  171. 171.
    Wang MH, Wang Y, Sun XZ, Cheng JS, Fu YP et al. 2015. Characterization of a novel megabirnavirus from Sclerotinia sclerotiorum reveals horizontal gene transfer from single-stranded RNA virus to double-stranded RNA virus. J. Virol. 89:8567–79
    [Google Scholar]
  172. 172.
    Watanabe T, Suzuki N, Tomonaga K, Sawa H, Matsuura Y et al. 2019. Neo-virology: the raison d'etre of viruses. Virus Res 274:197751
    [Google Scholar]
  173. 173.
    Wei S, Bian R, Andika IB, Niu E, Liu Q et al. 2019. Symptomatic plant viroid infections in phytopathogenic fungi. PNAS 116:13042–50
    [Google Scholar]
  174. 174.
    Wei S, Bian R, Andika IB, Niu E, Liu Q et al. 2020. Reply to Serra et al.: Nucleotide substitutions in plant viroid genomes that multiply in phytopathogenic fungi. PNAS 117:10129–30
    [Google Scholar]
  175. 175.
    Wickner RB, Fujimura T, Esteban R 2013. Viruses and prions of Saccharomyces cerevisiae. Adv. Virus Res. 86:1–36
    [Google Scholar]
  176. 176.
    Wolf YI, Kazlauskas D, Iranzo J, Lucia-Sanz A, Kuhn JH et al. 2018. Origins and evolution of the global RNA virome. mBio 9:e02329–18
    [Google Scholar]
  177. 177.
    Wu M, Deng Y, Zhou Z, He G, Chen W, Li G 2016. Characterization of three mycoviruses co-infecting the plant pathogenic fungus Sclerotinia nivalis. Virus Res 223:28–38
    [Google Scholar]
  178. 178.
    Xie J, Jiang D. 2014. New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu. Rev. Phytopathol. 52:45–68
    [Google Scholar]
  179. 179.
    Yaegashi H, Nakamura H, Sawahata T, Sasaki A, Iwanami Y et al. 2013. Appearance of mycovirus-like double-stranded RNAs in the white root rot fungus, Rosellinia necatrix, in an apple orchard. FEMS Microbiol. Ecol. 83:49–62
    [Google Scholar]
  180. 180.
    Yang M, Xu W, Zhou X, Yang Z, Wang Y et al. 2021. Discovery and characterization of a novel bipartite botrexvirus from the phytopathogenic fungus Botryosphaeria dothidea. Front. Microbiol. 12:696125
    [Google Scholar]
  181. 181.
    Yu J, Park JY, Heo JI, Kim KH. 2020. The ORF2 protein of Fusarium graminearum virus 1 suppresses the transcription of FgDICER2 and FgAGO1 to limit host antiviral defences. Mol. Plant Pathol. 21:230–43
    [Google Scholar]
  182. 182.
    Yu X, Li B, Fu Y, Jiang D, Ghabrial SA et al. 2010. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. PNAS 107:8387–92
    [Google Scholar]
  183. 183.
    Zerbini FM, Siddell SG, Mushegian AR, Walker PJ, Lefkowitz EJ et al. 2022. Differentiating between viruses and virus species by writing their names correctly. Arch. Virol. 167:1231–34
    [Google Scholar]
  184. 184.
    Zhai L, Xiang J, Zhang M, Fu M, Yang Z et al. 2016. Characterization of a novel double-stranded RNA mycovirus conferring hypovirulence from the phytopathogenic fungus Botryosphaeria dothidea. Virology 493:75–85
    [Google Scholar]
  185. 185.
    Zhang HX, Xie JT, Fu YP, Cheng JS, Qu Z et al. 2020. A 2-kb mycovirus converts a pathogenic fungus into a beneficial endophyte for Brassica protection and yield enhancement. Mol. Plant 13:1420–33
    [Google Scholar]
  186. 186.
    Zhang R, Hisano S, Tani A, Kondo H, Kanematsu S, Suzuki N. 2016. A capsidless ssRNA virus hosted by an unrelated dsRNA virus. Nat. Microbiol. 1:15001
    [Google Scholar]
  187. 187.
    Zhang S, Tian X, Navarro B, Di Serio F, Cao MJ. 2021. Watermelon crinkle leaf-associated virus 1 and watermelon crinkle leaf-associated virus 2 have a bipartite genome with molecular signatures typical of the members of the genus Coguvirus (family Phenuiviridae). Arch. Virol. 166:2829–34
    [Google Scholar]
  188. 188.
    Zhao L, Rosario K, Breitbart M, Duffy S 2019. Eukaryotic circular rep-encoding single-stranded DNA (CRESS DNA) viruses: ubiquitous viruses with small genomes and a diverse host range. Adv. Virus Res. 103:71–133
    [Google Scholar]
  189. 189.
    Zhou J, Hu X, Liang X, Wang Y, Xie C, Zheng L. 2021. Complete genome sequence of a novel mycovirus from Phoma matteucciicola. Arch. Virol. 166:317–20
    [Google Scholar]
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