Skip to main content
SpringerLink
Log in

Viruses infecting macrofungi

  • Review Article
  • Published:
VirusDisease Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Ever since their discovery just about 56 years ago in the cultivated mushroom Agaricus bisporus, many more viruses infecting fungi have been identified in a wide range of fungal taxa. With mostly being asymptomatic, especially the ones that are detrimental to their phytopathogenic hosts are intensively studied due to their considerable importance in developing novel plant protection measures. Contrary to the rapid accumulation of notable data on viruses of plant pathogenic microfungi, much less information have hitherto been obtained in regards to the viruses whose hosts are macrofungi. According to the current literature, only more than 80 distinct viruses bearing either linear dsRNA or linear positive sense ssRNA genome and infecting a total number of 34 macrofungal species represented with four Ascomycota and 30 Basidiomycota have been identified so far. Among these 34 macrofungal species, 14 are cultivated edible and wild edible mushroom species. According to the 10th ICTV (International Committee on Taxonomy of Viruses) Report, macrofungal viruses with linear dsRNA genome are classified into five families (Partitiviridae, Totiviridae, Chrysoviridae, Endornaviridae and Hypoviridae) and macrofungal viruses with linear positive sense ssRNA genome are classified into seven families (Betaflexiviridae, Gammaflexiviridae, Barnaviridae, Narnaviridae, Virgaviridae, Benyviridae and Tymoviridae). In this review, following a brief overview of some general characteristics of fungal viruses, an up to date knowledge on viruses infecting macrofungal hosts were presented by summarizing the previous, recent and prospective studies of the field.

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

  1. Bai X, Debaud JC, Schrunder J, Meinhardt F. The ectomycorrhizal basidiomycete Hebeloma circinans harbors a linear plasmid encoding a DNA- and RNA polymerase. J Gen Appl Microbiol. 1997;43:273–9. http://www.ncbi.nlm.nih.gov/pubmed/12501314.

  2. Barroso G, Labarère J. Evidence for viral and naked double-stranded RNAs in the basidiomycete Agrocybe aegerita. Curr Genet. 1990;18:231–7.

    Article  CAS  Google Scholar 

  3. Barton RJ, Hollings M. Purification and some properties of two viruses ınfecting the cultivated mushroom Agaricus bisporus. J Gen Virol. 1979;42:231–40.

    Article  CAS  Google Scholar 

  4. Blattny C, Kralik O. Virus Disease of Laccaria laccata (Scop. ex Fr.) cooke and some other fungi. Ces Mykol. 1968;22:161–6.

    Google Scholar 

  5. Burton K, Green J, Baker A, Eastwood D, Grogan H. Mushroom virus X—the identification of brown cap mushroom virus and a new highly sensitive diagnostic test for Phase III Compost. Reading. 2011;1990:466–73.

    Google Scholar 

  6. Chen K, Liang P, Chang ST, Yu ML. Volvariella volvacea virus—a new fungal dsRNA Virus from mushroom. Acta Microbiol Sin. 1988;28:19–23.

    Google Scholar 

  7. Chen K, Liang P, Yu M, Chang ST. A new double-stranded RNA virus from Volvariella volvacea. Mycologia. 1988;80:849–53.

    Article  CAS  Google Scholar 

  8. Dalman K, Olson A, Stenlid J. Evolutionary history of the conifer root rot fungus Heterobasidion annosum sensu lato. Mol Ecol. 2010;19:4979–93.

    Article  CAS  PubMed  Google Scholar 

  9. Deakin G, Dobbs E, Bennett JM, Jones IM, Grogan HM, Burton KS. Multiple viral infections in Agaricus bisporus—characterisation of 18 unique RNA viruses and 8 ORFans identified by deep sequencing. Sci Rep 2017;7:2469. http://www.ncbi.nlm.nih.gov/pubmed/28550284%0A; http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC5446422%0A; http://www.nature.com/articles/s41598-017-01592-9.

  10. Dieleman-van Zaayen M, Igesz O, Funch JT. Intracellular appearance and some mrophological features of viruslike particles in an ascomycete fungus. Virology. 1970;42:534–7.

    Article  Google Scholar 

  11. Dieleman-van Zaayen A. Mushroom virus disease in the Netherlands: symptoms, etiology, electron microscopy, spread and control. Institute of Phytopathological Research; 1972.

  12. Eastwood D, Green J, Grogan H, Burton K. Viral agents causing brown cap mushroom disease of Agaricus bisporus. Appl Environ Microbiol. 2015;81:7125–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Galagan JE, Selker EU. RIP: the evolutionary cost of genome defense. Trends Genet. 2004;20:417–23.

    Article  CAS  PubMed  Google Scholar 

  14. Gaze RH. Virus disease—Are you still there? Mushroom J. 1997;568:12–3.

    Google Scholar 

  15. Gaze RH, Calvo-Bado L, Challen MP, Adie BA, Romaine CP. A new virus disease of Agaricus bisporus. Mushroom Sci. 2000;15:701–5.

    Google Scholar 

  16. Ghabrial SA. New developments in fungal virology. Adv Virus Res. 1994;43:303–88.

    Article  CAS  PubMed  Google Scholar 

  17. Ghabrial SA, Castón JR, Jiang D, Nibert ML, Suzuki N. 50-Plus years of fungal viruses. Virology. 2015;479–480:356–68. https://doi.org/10.1016/j.virol.2015.02.034.

    Article  PubMed  Google Scholar 

  18. Ghabrial SA, Susuki N. Fungal viruses. 2008;2:284–91.

    Google Scholar 

  19. Ghabrial SA, Suzuki N. Viruses of plant pathogenic fungi. Annu Rev Phytopathol. 2009;47:353–84. https://doi.org/10.1146/annurev-phyto-080508-081932.

    Article  CAS  PubMed  Google Scholar 

  20. Go SJ, Park YH, Shin GC, Wessels JGH. Molecular analysis of double-stranded RNA in abnormal growing oyster mushroom, Pleurotus florida and Pleurotus ostreatus due to virus infection. Korean J Mycol. 1992;20:234–9.

    CAS  Google Scholar 

  21. Goodin MM, Schlagnhaufer B, Romaine CP. Encapsidation of the La France disease-specific double-stranded RNAs in 36 nm isometric virus-like particles. Phytopathology. 1992;82:285–90.

    Article  CAS  Google Scholar 

  22. Grogan HM, Adie BAT, Gaze RH, Challen MP, Mills PR. Double-stranded RNA elements associated with the MVX disease of Agaricus bisporus. Mycol Res 2003;107:147–54. http://linkinghub.elsevier.com/retrieve/pii/S0953756208611594.

  23. Guo M, Bian Y, Wang J, Wang G, Ma X, Xu Z. Biological and molecular characteristics of a novel partitivirus ınfecting the edible fungus Lentinula edodes. Plant Dis. 2017;101:726–33.

    Article  Google Scholar 

  24. Hane JK, Williams AH, Taranto AP, Solomon PS, Oliver RP. Repeat-induced point mutation in fungi: a fungal-specific endogenous mutagenesis process. In Genetic transformation systems in fungi. Springer; 2015. p. 55–68.

  25. Harmsen MC, Van Griensven LJLD, Wessels JGH. Molecular analysis of Agaricus bisporus double-stranded RNA. J Gen Virol. 1989;70:1613–6.

    Article  CAS  Google Scholar 

  26. Harmsen MC, Tolner B, Kram A, Go SJ, de Haan A, Wessels JGH. The Sequences of three dsRNAs associated with La France disease of the cultivated mushroom (Agaricus bisporus). Curr Genet. 1991;20:137–44.

    Article  CAS  PubMed  Google Scholar 

  27. Heinze C. A novel mycovirus from Clitocybe odora. Arch Virol. 2012;157:1831–4.

    Article  CAS  PubMed  Google Scholar 

  28. Hollings M. Viruses associated with a die-back disease of cultivated mushroom. Nature. 1962;196:962–5.

    Article  Google Scholar 

  29. Hollings M, Stone OM. Viruses that infect fungi. Annu Rev Phytopathol. 1971;9:93–118. https://doi.org/10.1146/annurev.py.09.090171.000521.

    Article  Google Scholar 

  30. Huttinga H, Wichers HJ, Dieleman-van Zaayen A. Filamentous and polyhedral virus-like particles in Boletus edulis. Neth J Plant Pathol. 1975;81:102–6.

    Article  Google Scholar 

  31. Hyder R, Pennanen T, Hamberg L, Vainio EJ, Piri T, Hantula J. Two viruses of Heterobasidion confer beneficial, cryptic or detrimental effects to their hosts in different situations. Fungal Ecol. 2013;6:387–96.

    Article  Google Scholar 

  32. Ihrmark K, Johannesson H, Stenström E, Stenlid J. Transmission of double-stranded RNA in Heterobasidion annosum. Fungal Genet Biol. 2002;36:147–54.

    Article  CAS  PubMed  Google Scholar 

  33. Ihrmark K, Stenström E, Stenlid J. Double-stranded RNA transmission through basidiospores of Heterobasidion annosum. Mycol Res. 2004;108:149–53.

    Article  CAS  PubMed  Google Scholar 

  34. Ihrmark K. Double-stranded RNA elements in the root rot fungus Heterobasidion annosum. Swedish University of Agricultural Sciences; 2001.

  35. Inouye T, Furuya K, Nisikado Y. Virus-like particles found in Shiitake. Ann Phytopathol Soc Jpn. 1970;36:356.

    Google Scholar 

  36. Jiang D, Fu Y, Guoqing L, Ghabrial SA. Viruses of the plant pathogenic fungus Sclerotinia sclerotiorum. Adv Virus Res. 2013. https://doi.org/10.1016/B978-0-12-394315-6.00008-8.

    PubMed  Google Scholar 

  37. Jurvansuu J, Kashif M, Vaario L, Vainio E, Hantula J. Partitiviruses of a fungal forest pathogen have species-specific quantities of genome segments and transcripts. Virology. 2014;462–463:25–33.

    Article  PubMed  Google Scholar 

  38. Kashif M, Hyder R, De Vega Perez D, Hantula J, Vainio EJ. Heterobasidion wood decay fungi host diverse and globally distributed viruses related to Helicobasidium mompa partitivirus V70. Virus Res. 2015;195:119–23.

    Article  CAS  PubMed  Google Scholar 

  39. Kim YJ, Kim JY, Kim JH, Yoon SM, Yoo YB, Yie SW. The identification of a novel Pleurotus ostreatus dsRNA virus and determination of the distribution of viruses in mushroom spores. J Microbiol. 2008;46:95–9.

    Article  CAS  PubMed  Google Scholar 

  40. Koltin Y, Perick R, Stamberg J, Shaul YB. Virus-like particles and cytoplasmic inheritance of plaques in a higher fungus. Nat New Biol. 1973;241:108–9.

    Article  CAS  PubMed  Google Scholar 

  41. Koons KK, Schlagnhaufer B, Romaine CP. Double-stranded RNAs in mycelial cultures of Agaricus bisporus affected by La France disease. Phytopathology. 1989;79:1272–5.

    Article  CAS  Google Scholar 

  42. Van der Lende TR, Duitman EH, Gunnewuk MGW, Yu L, Wessels JGH. Functional analysis of dsRNAs (L1, L2, L3, L5, and M2) associated with isometric 34-nm virions of Agaricus bisporus (white button mushroom). Virology. 1996;217:88–96.

    Article  PubMed  Google Scholar 

  43. van der Lende TR, Harmsen MC, Go SJ, Wessel JGH. Double-stranded RNA mycoviruses in mycelium of Pleurotus ostreatus. FEMS Microbiol Lett. 1995;125:51–6.

    Article  PubMed  Google Scholar 

  44. Van der Lende TR, Harmsen MC, Wessels JGH. Double-stranded RNAs and proteins associated with the 34 nm virus particles of the cultivated mushroom Agaricus bisporus. J Gen Virol. 1994;75:2533–6.

    Article  PubMed  Google Scholar 

  45. Lim W, Jeong JH, Jeong R-D, Yoo YB, Yie SW, Kim K-H. Complete nucleotide sequence and genome organization of a dsRNA partitivirus infecting Pleurotus ostreatus. Virus Res. 2005;108:111–9. http://linkinghub.elsevier.com/retrieve/pii/S0168170204003399.

  46. Maffettone E. Characterization of a novel virus associated with the MVX disease of Agaricus bisporus. Cranfield University; 2007. https://dspace.lib.cranfield.ac.uk/handle/1826/2956.

  47. Magae Y, Hayashi N. Double-stranded RNA and virus-like particles in the edible basidiomycete Flammulina velutipes (Enokitake). FEMS Microbiol Lett. 1999;180:331–5.

    Article  CAS  PubMed  Google Scholar 

  48. Magae Y, Sunagawa M. Characterization of a mycovirus associated with the brown discoloration of edible mushroom, Flammulina velutipes. Virol J. 2010;7:342.

    PubMed  PubMed Central  Google Scholar 

  49. Magae Y. Molecular characterization of a novel mycovirus in the cultivated mushroom, Lentinula edodes. Virol J 2012;9:60. http://virologyj.biomedcentral.com/articles/10.1186/1743-422X-9-60.

  50. Marquez LM, Redman RS, Rodriguez RJ, Roossinck MJ. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science. 2007;315:513–5. https://doi.org/10.1126/science.1136237.

    Article  CAS  PubMed  Google Scholar 

  51. Mori K, Kuida K, Hosokama D, Takehara M. Virus-like particles in several mushrooms. Mushroom Sci. 1978;10:773–87.

    Google Scholar 

  52. Nibert ML, Ghabrial SA, Maiss E, Lesker T, Vainio EJ, Jiang D, et al. Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res. 2014;188:128–41. https://doi.org/10.1016/j.virusres.2014.04.007.

    Article  CAS  PubMed  Google Scholar 

  53. Ohta C, Taguchi T, Takahashi S, Ohtsuka K, Eda K, Ayusawa S, Magae Y. Detection of double stranded RNA elements in cultivated Lentinula edodes. Mushroom Sci Biotechnol. 2008;16:155–8.

    Google Scholar 

  54. Olson Å, Aerts A, Asiegbu F, Belbahri L, Bouzid O, Broberg A, et al. Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen. New Phytol. 2012;194:1001–13.

    Article  PubMed  Google Scholar 

  55. Paoletti M. Vegetative incompatibility in fungi: from recognition to cell death, whatever does the trick. Fungal Biol Rev. 2016;30:152–62.

    Article  Google Scholar 

  56. Park JS, Kim YH. Infectious RNA viruses in the edible mushroom Pleurotus spp. J Microbiol. 1996;34:61–76.

    Google Scholar 

  57. Pearson MN, Beever RE, Boine B, Arthur K. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol. 2009;10:115–28.

    Article  CAS  PubMed  Google Scholar 

  58. Petrzik K, Sarkisova T, Starý J, Koloniuk I, Hrabáková L, Kubešová O. Molecular characterization of a new monopartite dsRNA mycovirus from mycorrhizal Thelephora terrestris (Ehrh.) and its detection in soil oribatid mites (Acari: Oribatida). Virology. 2016;489:12–9.

    Article  CAS  PubMed  Google Scholar 

  59. Pingyan L, Hongdi L, Kaiying C. Intracellular appearance, morphological features and properties of oyster mushroom virus. Mycol Res. 1990;94:529–37. https://doi.org/10.1016/S0953-7562(10)80016-4.

    Article  Google Scholar 

  60. Power AG, Mitchell CE. Pathogen spillover in disease epidemics. Am Nat. 2004;164(Suppl):S79–89.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  62. Rao JR, Nelson DWA, McClean S. The enigma of double-stranded RNA (dsRNA) associated with mushroom virus X (MVX). Curr Issues Mol Biol. 2007;9:103–22.

    CAS  PubMed  Google Scholar 

  63. Revill PA, Davidson AD, Wright PJ. The nucleotide sequence and genome organization of mushroom bacilliform virus: a single-stranded RNA virus of Agaricus bisporus (Lange) Imbach. Virology. 1994;202:904–11.

    Article  CAS  PubMed  Google Scholar 

  64. Ro HS, Kang EJ, Yu JS, Lee TS, Lee CW, Lee HS. Isolation and characterization of a novel mycovirus, PeSV, in Pleurotus eryngii and the development of a diagnostic system for it. Biotechnol Lett. 2007;29:129–35.

    Article  CAS  PubMed  Google Scholar 

  65. Ro HS, Lee NJ, Lee CW, Lee HS. Isolation of a novel mycovirus OMIV in Pleurotus ostreatus and its detection using a triple antibody sandwich-ELISA. J Virol Methods. 2006;138:24–9.

    Article  CAS  PubMed  Google Scholar 

  66. Romaine CP, Schlagnhaufer B. Prevalence of dsRNAs in healthy and La France disease-affected basidiocarps of Agaricus bisporus. Mycologia. 1989;81:822–5.

    Article  CAS  Google Scholar 

  67. Romaine CP, Ulhrich P, Schlagnhaufer B. Transmission of La France isometric virus during basidiosporogenesis in Agaricus bisporus. Mycologia. 1993;85:175–9.

    Article  Google Scholar 

  68. Romaine CP, Goodin M. Unravelling the viral complex associated with La France disease of the cultivated mushroom, Agaricus bisporus. dsRNA Genet. Elem. Concepts Appl. CRC Press LLC; 2002. p. 237–57.

  69. Rong R, Rao S, Scott SW, Tainter FH. Common multiple dsRNAs are present in populations of the fungus Discula destructiva originating from widely separated geographic locations. Curr Microbiol. 2001;42:144–8.

    CAS  PubMed  Google Scholar 

  70. Roossinck MJ. Lifestyles of plant viruses. Philos Trans R Soc B Biol Sci. 2010;365:1899–905. https://doi.org/10.1098/rstb.2010.0057.

    Article  Google Scholar 

  71. Rytter JL, Royse DJ, Romaine CP. Incidence and diversity of double-stranded RNA in Lentinula edodes. Mycologia. 1991;83:506–10.

    Article  CAS  Google Scholar 

  72. Sasaki A, Kanematsu S, Onoue M, Oyama Y, Yoshida K. Infection of Rosellinia necatrix with purified viral particles of a member of Partitiviridae (RnPV1-W8). Arch Virol. 2006;151:697–707.

    Article  CAS  PubMed  Google Scholar 

  73. Schelhaas MJ, Nabuurs GJ, Schuck A. Natural disturbances in the European forests in the 19th and 20th centuries. Glob Chang Biol. 2003;9:1620–33. https://doi.org/10.1046/j.1365-2486.2003.00684.x.

    Article  Google Scholar 

  74. Schisler LC, Sinden JW, Sigel EM. Etiology, symptomatology and epidemiology of a virus disease of cultivated mushrooms. Phytopathology. 1967;57:519–26.

    Google Scholar 

  75. Servi H, Akata I, Çetin B. Macrofungal diversity of Bolu Abant Nature Park. Afr J Biotechnol. 2010;9:3622–8.

    Google Scholar 

  76. Shahriari H, Kirkham JB, Casselton LA. Virus-like particles in the fungus Coprinus lagopus. Heredity (Edinb). 1973;31:428.

    Google Scholar 

  77. Shamoun SF, Varga A, Valverde RA, Ramsfield T, Sumampong G, Elliott M, et al. Identification and molecular characterization of a new double-stranded RNA virus infecting Chondrostereum purpureum. Can J Plant Pathol. 2008;30:604–13.

    Article  CAS  Google Scholar 

  78. Sinden JW, Hauser E. Report on two new mushroom diseases. Mushroom Sci. 1950;1:96–100.

    Google Scholar 

  79. Sonnenberg AS, Lavrijssen B. Browning of mushroom and the presence of viral double-stranded RNA in Dutch mushrooms. In: Keil CB, Rinker DLRD, editors. Science cultivated edible medicinal fungi. State College: Penn State University; 2004. p. 541–6.

    Google Scholar 

  80. Sonnenberg AS, Van Griensven LJLD. Evidence for transmission of La France disease in Agaricus bisporus by dsRNA. Genet. Breed. Agaricus. 1991. p. 109–13.

  81. Stenlid J, Redfern DB. Spread within the tree and stand Heterobasidion annosum. Biology, ecology, impact and Control. Wallingford: CAB International; 1998. p. 125–41.

  82. Stielow JB, Bratek Z, Klenk HP, Winter S, Menzel W. A novel mitovirus from the hypogeous ectomycorrhizal fungus Tuber excavatum. Arch Virol. 2012;157:787–90.

    Article  CAS  PubMed  Google Scholar 

  83. Stielow B, Klenk HP, Menzel W. Complete genome sequence of the first endornavirus from the ascocarp of the ectomycorrhizal fungus Tuber aestivum Vittad. Arch Virol. 2011;156:343–5.

    Article  CAS  PubMed  Google Scholar 

  84. Stielow B, Klenk HP, Winter S, Menzel W. A novel Tuber aestivum (Vittad.) mitovirus. Arch Virol. 2011;156:1107–10.

    Article  CAS  PubMed  Google Scholar 

  85. Stielow B, Menzel W. Complete nucleotide sequence of TaV1, a novel totivirus isolated from a black truffle ascocarp (Tuber aestivum Vittad.). Arch Virol. 2010;155:2075–8.

    Article  CAS  PubMed  Google Scholar 

  86. Ushiyama R, Nakai Y. Intracellular virus-like particles in Lentinus edodes. J Gen Virol. 1980;46:507–9.

    Article  Google Scholar 

  87. Ushiyama R, Nakai Y. Ultrastructural features of fungal virus-like particles from Lentinus edodes. Virology. 1982;123:93–101.

    Article  CAS  PubMed  Google Scholar 

  88. Ushiyama R, Nakai Y, Ikegami M. Evidence for double-stranded RNA from polyhedral virus-like particles in Lentinus edodes (Berk.) Sing. Virology. 1977;77:880–3.

    Article  CAS  PubMed  Google Scholar 

  89. Vainio EJ, Capretti P, Motta E, Hantula J. Molecular characterization of HetRV8-ir1, a partitivirus of the invasive conifer pathogenic fungus Heterobasidion irregulare. Arch Virol. 2013;158:1613–5.

    Article  CAS  PubMed  Google Scholar 

  90. Vainio EJ, Hakanpää J, Dai YC, Hansen E, Korhonen K, Hantula J. Species of Heterobasidion host a diverse pool of partitiviruses with global distribution and interspecies transmission. Fungal Biol. 2011;115:1234–43.

    Article  CAS  PubMed  Google Scholar 

  91. Vainio EJ, Hyder R, Aday G, Hansen E, Piri T, Doǧmuş-Lehtijärvi T, et al. Population structure of a novel putative mycovirus infecting the conifer root-rot fungus Heterobasidion annosum sensu lato. Virology. 2012;422:366–76.

    Article  CAS  PubMed  Google Scholar 

  92. Vainio EJ, Jurvansuu J, Streng J, Rajamäki ML, Hantula J, Valkonen JPT. Diagnosis and discovery of fungal viruses using deep sequencing of small RNAs. J Gen Virol. 2015;96:714–25.

    Article  CAS  PubMed  Google Scholar 

  93. Vainio EJ, Keriö S, Hantula J. Description of a new putative virus infecting the conifer pathogenic fungus Heterobasidion parviporum with resemblance to Heterobasidion annosum P-type partitivirus. Arch Virol. 2011;156:79–86.

    Article  CAS  PubMed  Google Scholar 

  94. Vainio EJ, Korhonen K, Tuomivirta TT, Hantula J. A novel putative partitivirus of the saprotrophic fungus Heterobasidion ecrustosum infects pathogenic species of the Heterobasidion annosum complex. Fungal Biol. 2010;114:955–65. https://doi.org/10.1016/j.funbio.2010.09.006.

    Article  CAS  PubMed  Google Scholar 

  95. Vainio EJ, Pennanen T, Rajala T, Hantula J. Occurrence of similar mycoviruses in pathogenic, saprotrophic and mycorrhizal fungi inhabiting the same forest stand. FEMS Microbiol Ecol. 2017;110:fix003. https://doi.org/10.1093/femsec/fix003.

    Article  Google Scholar 

  96. Vainio EJ, Piri T, Hantula J. Virus community dynamics in the conifer pathogenic fungus heterobasidion parviporum following an artificial introduction of a partitivirus. Microb Ecol. 2013;65:28–38.

    Article  CAS  PubMed  Google Scholar 

  97. Vainio EJ, Müller MM, Korhonen K, Piri T, Hantula J. Viruses accumulate in aging infection centers of a fungal forest pathogen. ISME J. 2014;1–11. http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej2014145a.html?WT.mc_id=TWT_ISMEJ.

  98. Wach MP, Sriskantha A, Romaine CP. Double-stranded RNAs associated with La France disease of the commercial mushroom. Phytopathology. 1987;77:1321–5.

    Article  CAS  Google Scholar 

  99. Wang M, Wang Y, Sun X, Cheng J, Fu Y, Liu H, et al. Characterization of a novel megabirnavirus from Sclerotinia sclerotiorum reveals horizontal gene transfer from single-stranded RNA virus to double-stranded RNA virus. J Virol. 2015;89:8567–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Won HK, Park SJ, Kim DK, Shin MJ, Kim N, Lee SH, et al. Isolation and characterization of a mycovirus in Lentinula edodes. J Microbiol. 2013;51:118–22.

    Article  CAS  PubMed  Google Scholar 

  101. Woodward S, Stenlid J, Karjalainen R, Hutterman A. Heterobasidion annosum. Biology, ecology, impact and control. Wallingford: CAB International; 1998.

  102. Wyn-Jones AP, Whalley AJS. Virus-like particles in hypoxylon multiforme. Mycopathologia. 1977;61:63–4.

    Article  Google Scholar 

  103. Xueren S, Mingjie C, Juying S, Yangjie P, Zuxun G. The detection of single-stranded RNA in an isometric virus-like particle from Shiitake mushroom [Lentinus edodes (Berk.) Sing.]. Ann Appl Biol. 1993;122:271–7.

    Article  Google Scholar 

  104. Yu HJ, Lim D, Lee HS. Characterization of a novel single-stranded RNA mycovirus in Pleurotus ostreatus. Virology. 2003;314:9–15.

    Article  CAS  PubMed  Google Scholar 

  105. Van Zaayen A. Mushroom viruses. In: Lemke PA, editor. Viruses and plasmids in fungi. New York: Marcel Dekker Inc; 1979. p. 239–324.

    Google Scholar 

Download references

Acknowledgements

Part of this study was orally presented in the 1st International Eurasia Mycology Congress which was held in Manisa/Turkey on the 3th–5th of July 2017.

Author information

Authors and Affiliations

  1. Faculty of Science, Department of Biology, Ankara University, Ankara, Turkey

    Ergin Sahin & Ilgaz Akata

Authors
  1. Ergin Sahin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ilgaz Akata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ergin Sahin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sahin, E., Akata, I. Viruses infecting macrofungi. VirusDis. 29, 1–18 (2018). https://doi.org/10.1007/s13337-018-0434-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13337-018-0434-8

Keywords

Search

Navigation