Skip to main content

Diversity of mycoviruses in edible fungi

Abstract

Mycoviruses (fungal viruses) are widespread in all major taxonomic groups of fungi. Although most mycovirus infections are latent, some mycoviruses, such as La France isometric virus, mushroom virus X, and oyster mushroom spherical virus, can cause severe diseases in edible fungi and lead to significant production losses. Recently, deep sequencing has been employed as a powerful research tool to identify new mycoviruses and to enhance our understanding of virus diversity and evolution. An increasing number of novel mycoviruses that can infect edible fungi have been reported, including double-stranded (ds) RNA, positive-sense ( +)ssRNA, and negative-sense (−)ssRNA viruses. To date, approximately 60 mycoviruses have been reported in edible fungi. In this review, we summarize the recent advances in the diversity and evolution of mycoviruses that can infect edible fungi. We also discuss mycovirus transmission, co-infections, and genetic variations, as well as the methods used to detect and control of mycoviruses in edible fungi, and provide insights for future research on mushroom viral diseases.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Hollings M (1962) Viruses associated with a die-back disease of cultivated mushroom. Nature 196:962–965. https://doi.org/10.1038/196962a0

    Article  Google Scholar 

  2. Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384. https://doi.org/10.1146/annurev-phyto-080508-081932

    CAS  Article  PubMed  Google Scholar 

  3. Ghabrial SA, Castón JR, Jiang DH, Nibert ML, Suzuki N (2015) 50-plus years of fungal viruses. Virology 479–480:356–368. https://doi.org/10.1016/j.virol.2015.02.034

    CAS  Article  PubMed  Google Scholar 

  4. Xie JT, Jiang DH (2014) New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52:45–68. https://doi.org/10.1146/annurev-phyto-102313-050222

    CAS  Article  PubMed  Google Scholar 

  5. Son M, Yu J, Kim KH (2015) Five questions about mycoviruses. PLoS Pathog 11(11):e1005172. https://doi.org/10.1371/journal.ppat.1005172

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Nuss DL (2005) Hypovirulence: Mycoviruses at the fungal–plant interface. Nat Rev Microbiol 3(8):632–642. https://doi.org/10.1038/nrmicro1206

    CAS  Article  PubMed  Google Scholar 

  7. Rao JR, Nelson DW, McClean S (2007) The enigma of double-stranded RNA (dsRNA) associated with mushroom virus X (MVX). Curr Issues Mol Biol 9(2):103–121

    CAS  PubMed  Google Scholar 

  8. Goodin MM, Schlagnhaufer B, Romaine CP (1992) Encapsidation of the La France disease-specific double-stranded RNAs in 36-nm isometric virus like particles. Phytopathology 82(3):285–290. https://doi.org/10.1094/phyto-82-285

    CAS  Article  Google Scholar 

  9. Yu HJ, Lim D, Lee HS (2003) Characterization of a novel single-stranded RNA mycovirus in Pleurotus ostreatus. Virology 314:9–15. https://doi.org/10.1016/S0042-6822(03)00382-9

    CAS  Article  PubMed  Google Scholar 

  10. Pearson M, Beever R, Boine B, Arthur K (2009) Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol 10(1):115–128. https://doi.org/10.1111/j.1364-3703.2008.00503.x

    CAS  Article  PubMed  Google Scholar 

  11. Wolf YI, Kazlauskas D, Iranzo J, Lucía-Sanz A, Kuhn JH, Krupovic M, Dolja VV, Koonin EV (2018) Origins and evolution of the global RNA virome. MBio 9:e02329-e2318. https://doi.org/10.1128/mBio.02329-18

    Article  PubMed  PubMed Central  Google Scholar 

  12. Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI, Yutin N, Zerbini FM, Kuhn JH (2020) Global organization and proposed megataxonomy of the virus world. Microbiol Mol Biol Rev 84(2):e00061-e119. https://doi.org/10.1128/MMBR.00061-19

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Yu X, Li B, Fu YP, Jiang DH, Ghabrial SA, Li GQ, Peng YL, Xie JT, Cheng JS, Huang JB, Yi XH (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107(18):8387–8392. https://doi.org/10.1073/pnas.0913535107

    Article  PubMed  PubMed Central  Google Scholar 

  14. 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(14):eaay9634. https://doi.org/10.1126/sciadv.aay9634

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Marzano SL, Nelson BD, Ajayi-Oyetunde O, Bradley CA, Hughes TJ, Hartman GL, Eastburn DM, Domier LL (2016) Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J Virol 90(15):6846–6863. https://doi.org/10.1128/JVI.00357-16

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Dudas G, Huber G, Wilkinson M, Yllanes D (2021) Polymorphism of genetic ambigrams. Virus Evol 7(1):038. https://doi.org/10.1093/ve/veab038

    Article  Google Scholar 

  17. Sato Y, Shamsi W, Jamal A, Bhatti MF, Kondo H, Suzuki N, Wickner RB (2020) Hadaka virus 1: a capsidless eleven-segmented positive-sense-single-stranded RNA virus from a phytopathogenic fungus Fusarium oxysporum. MBio 11(3):e00450. https://doi.org/10.1128/mBio.00450-20

    Article  PubMed  PubMed Central  Google Scholar 

  18. 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(1):15001. https://doi.org/10.1038/nmicrobiol.2015.1

    CAS  Article  PubMed  Google Scholar 

  19. Jia HX, Dong KL, Zhou LL, Wang GP, Hong N, Jiang DH, Xu WX (2017) A dsRNA virus with filamentous viral particles. Nat Commun 8(1):168. https://doi.org/10.1038/s41467-017-00237-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Kanhayuwa L, Kotta-Loizou I, Özkan S, Gunning AP, Coutts RH (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(29):9100–9105. https://doi.org/10.1073/pnas.1419225112

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Kotta-Loizou I (2021) Mycoviruses and their role in fungal pathogenesis. Curr Opin Microbiol 63:10–18. https://doi.org/10.1016/j.mib.2021.05.007

    CAS  Article  PubMed  Google Scholar 

  22. Vainio EJ, Chiba S, Ghabrial SA, Maiss E, Roossinck M, Sabanadzovic S, Suzuki N, Xie J, Nibert M, Ictv Report C (2018) ICTV virus taxonomy profile: Partitiviridae. J Gen Virol 99(1):17–18. https://doi.org/10.1099/jgv.0.000985

    CAS  Article  PubMed  Google Scholar 

  23. Magae Y (2012) Molecular characterization of a novel mycovirus in the cultivated mushroom, Lentinula edodes. Virol J 9(1):60. https://doi.org/10.1186/1743-422X-9-60

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ohta C, Taguchi T, Takahashi S, Ohtsuka K, Eda K, Ayusawa S, Magae Y (2008) Detection of double stranded RNA elements in cultivated Lentinula edodes (in Japanese). Mushroom Sci Biotechnol 16:155–158

    Google Scholar 

  25. Won HK, Park SJ, Kim DK, Shin M, Kim N, Lee SH, Kwon YC, Ko H, Ro HS, Lee HS (2013) Isolation and characterization of a mycovirus in Lentinula edodes. J Microbiol 51:118–122. https://doi.org/10.1007/s12275-013-2351-2

    CAS  Article  PubMed  Google Scholar 

  26. Petrzik K, Sarkisova T, Starý J, Koloniuk I, Hrabáková L, Kubešová O (2016) Molecular characterization of a new monopartite dsRNA mycovirus from mycorrhizal Thelephora terrestris (Ehrh.) and its detection in soil oribatid mites (Acari: Oribatida). Virology 489:12–19. https://doi.org/10.1016/j.virol.2015.11.009

    CAS  Article  PubMed  Google Scholar 

  27. Picarelli M, Forgia M, Rivas EB, Nerva L, Chiapello M, Turina M, Colariccio A (2019) Extreme diversity of mycoviruses present in isolates of Rhizoctonia solani AG2-2 LP From Zoysia japonica from Brazil. Front Cell Infect Microbiol 9:244. https://doi.org/10.3389/fcimb.2019.00244

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Zhang R, Liu S, Chiba S, Kondo H, Kanematsu S, Suzuki N (2014) A novel single-stranded RNA virus isolated from a phytopathogenic filamentous fungus, Rosellinia necatrix, with similarity to hypo-like viruses. Front Microbiol 5:360. https://doi.org/10.3389/fmicb.2014.00360

    Article  PubMed  PubMed Central  Google Scholar 

  29. Ayllón MA, Turina M, Xie JT, Nerva L, Marzano S-YL, Donaire L, Jiang DH, Consortium IR (2020) ICTV virus taxonomy profile: Botourmiaviridae. J Gen Virol 101(5):454–455. https://doi.org/10.1099/jgv.0.001409

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Lin YH, Fujita M, Chiba S, Hyodo K, Andika IB, Suzuki N, Kondo H (2019) Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes). Virology 533:125–136. https://doi.org/10.1016/j.virol.2019.05.008

    CAS  Article  PubMed  Google Scholar 

  31. Vainio EJ, Sutela S (2020) Mixed infection by a partitivirus and a negative-sense RNA virus related to mymonaviruses in the polypore fungus Bondarzewia berkeleyi. Virus Res 286:198079. https://doi.org/10.1016/j.virusres.2020.198079

    CAS  Article  PubMed  Google Scholar 

  32. Guo MP, Shen GY, Wang JJ, Liu MJ, Bian YB, Xu ZY (2021) Mycoviral diversity and characteristics of a negative-stranded RNA virus LeNSRV1 in the edible mushroom Lentinula edodes. Virology 555:89–101. https://doi.org/10.1016/j.virol.2020.11.008

    CAS  Article  PubMed  Google Scholar 

  33. Rigling D, Prospero S (2018) Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Mol Plant Pathol 19(1):7–20. https://doi.org/10.1111/mpp.12542

    CAS  Article  PubMed  Google Scholar 

  34. Yu X, Li B, Fu YP, Xie JT, Cheng JS, Ghabrial SA, Li GQ, Yi XH, Jiang DH (2013) Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proc Natl Acad Sci USA 110(4):1452–1457. https://doi.org/10.1073/pnas.1213755110

    Article  PubMed  PubMed Central  Google Scholar 

  35. Shah UA, Kotta-Loizou I (2020) Mycovirus-induced hypervirulence of Leptosphaeria biglobosa enhances systemic acquired resistance to Leptosphaeria maculans in Brassica napus. Mol Plant Microbe Interact 33(1):98–107. https://doi.org/10.1094/mpmi-09-19-0254-r

    CAS  Article  PubMed  Google Scholar 

  36. Kotta-Loizou I, Coutts RH (2017) Studies on the virome of the entomopathogenic fungus Beauveria bassiana reveal ovnel dsRNA elements and mild hypervirulence. PLoS Pathog 13(1):e1006183. https://doi.org/10.1371/journal.ppat.1006183

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Özkan S, Coutts RH (2015) Aspergillus fumigatus mycovirus causes mild hypervirulent effect on pathogenicity when tested on Galleria mellonella. Fungal Genet Biol 76:20–26. https://doi.org/10.1016/j.fgb.2015.01.003

    Article  PubMed  Google Scholar 

  38. Lau SP, Lo GS (2018) Novel partitivirus enhances virulence of and causes aberrant gene expression in Talaromyces marneffei. MBio 9(3):e00947-e918. https://doi.org/10.1128/mBio.00947-18

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Romaine C, Goodin M (2002) Unraveling the viral complex associated with La France disease of the cultivated mushroom, Agaricus bisporus. DsRNA Genetic Elements. https://doi.org/10.1201/9781420039122

    Article  Google Scholar 

  40. O’Connor E, Doyle S, Amini A, Grogan H, Fitzpatrick DA (2021) Transmission of mushroom virus X and the impact of virus infection on the transcriptomes and proteomes of different strains of Agaricus bisporus. Fungal Biol 125(9):704–717. https://doi.org/10.1016/j.funbio.2021.04.005

    CAS  Article  PubMed  Google Scholar 

  41. Song HY, Kim N, Kim DH, Kim JM (2020) The PoV mycovirus affects extracellular enzyme expression and fruiting body yield in the oyster mushroom, Pleurotus ostreatus. Sci Rep 10(1):1094. https://doi.org/10.1038/s41598-020-58016-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Hillman BI, Annisa A, Suzuki N (2018) Chapter Five - Viruses of plant-interacting fungi, In: Advances in Virus Research, Academic Press. pp 99–116.

  43. Thapa V, Roossinck MJ (2019) Determinants of coinfection in the mycoviruses. Front Cell Infect Microbiol 9:169. https://doi.org/10.3389/fcimb.2019.00169

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. van Diepeningen AD, Debets AJM, Hoekstra RF (1997) Heterokaryon incompatibility blocks virus transfer among natural isolates of black Aspergilli. Curr Genet 32(3):209–217. https://doi.org/10.1007/s002940050268

    Article  PubMed  Google Scholar 

  45. Wu SS, Cheng JS, Fu YP, Chen T, Jiang DH, Ghabrial SA, Xie JT (2017) Virus-mediated suppression of host non-self recognition facilitates horizontal transmission of heterologous viruses. PLoS Pathog 13(3):e1006234. https://doi.org/10.1371/journal.ppat.1006234

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Andika IB, Kondo H, Suzuki N (2019) Dicer functions transcriptionally and posttranscriptionally in a multilayer antiviral defense. Proc Natl Acad Sci USA 116(6):2274–2281. https://doi.org/10.1073/pnas.1812407116

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. 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. https://doi.org/10.1016/j.virol.2019.05.004

    CAS  Article  PubMed  Google Scholar 

  48. 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(2):100. https://doi.org/10.3390/biology10020100

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Sun LY, Suzuki N (2008) Intragenic rearrangements of a mycoreovirus induced by the multifunctional protein p29 encoded by the prototypic hypovirus CHV1-EP713. RNA 14(12):2557–2571. https://doi.org/10.1261/rna.1125408

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Guo MP, Bian YB, Wang JJ, Wang GZ, Ma XH, Xu ZY (2017) Biological and molecular characteristics of a novel partitivirus infecting the edible fungus Lentinula edodes. Plant Dis 101(5):726–733. https://doi.org/10.1094/PDIS-07-16-0951-RE

    CAS  Article  PubMed  Google Scholar 

  51. Kim E, Park MJ, Jang Y, Ryoo R, Ka KH (2021) Detection of RNA mycoviruses in wild strains of Lentinula edodes in Korea. Korean J Mycol 49(3):285–294

    Google Scholar 

  52. Liu S, Xie JT, Cheng JS, Li B, Chen T, Fu YP, Li GQ, Wang MQ, Jin HN, Wan H, Jiang DH (2016) Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector. Proc Natl Acad Sci USA 113(45):12803–12808. https://doi.org/10.1073/pnas.1608013113

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Romaine CP, Ulhrich P, Schlagnhaufer B (1993) Transmission of La France isometric virus during basidiosporogenesis in Agaricus bisporus. Mycologia 85(2):175–179. https://doi.org/10.1080/00275514.1992.12026264

    Article  Google Scholar 

  54. Wang JJ, Guo MP, Sun YJ, Bian YB, Zhou Y, Xu ZY (2018) Genetic variation and phylogenetic analyses reveal transmission clues of Lentinula edodes partitivirus 1 (LePV1) from the Chinese L. edodes core collection. Virus Res 255:127–132. https://doi.org/10.1016/j.virusres.2018.07.012

    CAS  Article  PubMed  Google Scholar 

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

    Google Scholar 

  56. Ghabrial SA (1994) New developments in fungal virology. Adv Virus Res 43:303–388. https://doi.org/10.1016/s0065-3527(08)60052-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. van der Lende TR, Harmsen MC, Wessels JGH (1994) Double-stranded RNAs and proteins associated with the 34 nm virus particles of the cultivated mushroom Agaricus bisporus. J Gen Virol 75(9):2533–2536. https://doi.org/10.1099/0022-1317-75-9-2533

    Article  PubMed  Google Scholar 

  58. Van Der Lende TR, Duitman EH, Gunnewijk MGW, Yu LI, Wessels JGH (1996) Functional analysis of dsRNAs (L1, L3, L5, and M2) associated with isometric 34-nm virions of Agaricus bisporus (White button mushroom). Virology 217(1):88–96. https://doi.org/10.1006/viro.1996.0096

    Article  PubMed  Google Scholar 

  59. Harmsen M, Van Griensven L, Wessels J (1989) Molecular analysis of Agaricus bisporus double-stranded RNA. J Gen Virol 70:1613–1616. https://doi.org/10.1099/0022-1317-70-6-1613

    CAS  Article  Google Scholar 

  60. Koons K, Schlagnhaufer B, Romaine C (1989) Double-stranded RNAs in mycelial cultures of Agaricus bisporus affected by La France disease. Phytopathology 79(11):1272–1275. https://doi.org/10.1094/phyto-79-1272

    CAS  Article  Google Scholar 

  61. Harmsen MC, Tolner B, Kram A, Go SJ, de Haan A, Wessels JGH (1991) Sequences of three dsRNAs associated with La France disease of the cultivated mushroom (Agaricus bisporus). Curr Genet 20(1):137–144. https://doi.org/10.1007/BF00312776

    CAS  Article  PubMed  Google Scholar 

  62. Tavantzis SM, Romaine CP, Smith SH (1980) Purification and partial characterization of a bacilliform virus from Agaricus bisporus: a single-stranded RNA mycovirus. Virology 105(1):94–102. https://doi.org/10.1016/0042-6822(80)90159-2

    CAS  Article  PubMed  Google Scholar 

  63. Revill PA, Davidson AD, Wright PJ (1994) The nucleotide sequence and genome organization of mushroom bacilliform virus: a single-stranded RNA virus of Agaricus bisporus (Lange) Imbach. Virology 202(2):904–911. https://doi.org/10.1006/viro.1994.1412

    CAS  Article  PubMed  Google Scholar 

  64. 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(1):2469. https://doi.org/10.1038/s41598-017-01592-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Revill PA, Davidson AD, Wright PJ (1999) Identification of a subgenomic mRNA encoding the capsid protein of mushroom bacilliform virus, a single-stranded RNA mycovirus. Virology 260(2):273–276. https://doi.org/10.1006/viro.1999.9839

    CAS  Article  PubMed  Google Scholar 

  66. Gaze RH (1997) Virus disease-Are you still there? Mushroom J 568:12–13

    Google Scholar 

  67. Gaze RH, Calvo-Bado L, Challen M, Adie B, Romaine C (2000) A new virus disease of Agaricus bisporus? Sci Cultivat Edible Fungi Balkema 2:701–705

    Google Scholar 

  68. Sonnenberg AS, Lavrijssen B (2004) Browning of mushroom and the presence of viral double-stranded RNA in Dutch mushrooms. Mushroom Sci 541–546

  69. Pudełko K (2010) Mushroom virus X (MVX): a novel disease of mushrooms in Poland? J Plant Prot Res 50(3):366–371. https://doi.org/10.2478/v10045-010-0062-9

    Article  Google Scholar 

  70. Halász K, Geösel A, Szarvas J, Virágh N, Hajdú C, Lukács N (2014) Occurrence of double-stranded RNA species in champignon and their relation to mushroom virus X symptoms. Acta Aliment 43:592–603. https://doi.org/10.1556/AAlim.2013.0009

    Article  Google Scholar 

  71. Grogan HM, Adie BT, Gaze RH, Challen MP, Mills PR (2003) Double-stranded RNA elements associated with the MVX disease of Agaricus bisporus. Mycol Res 107(2):147–154. https://doi.org/10.1017/S0953756203007202

    CAS  Article  PubMed  Google Scholar 

  72. Dobbs E, Deakin G, Bennett J, Fleming-Archibald C, Burton K (2021) Viral interactions and pathogenesis during multiple viral infections in Agaricus bisporus. MBio 12(1):e03470. https://doi.org/10.1128/mBio.03470-20

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Fleming-Archibald C, Ruggiero A, Grogan HM (2015) Brown mushroom symptom expression following infection of an Agaricus bisporus crop with MVX associated dsRNAs. Fungal Biol 119(12):1237–1245. https://doi.org/10.1016/j.funbio.2015.09.004

    CAS  Article  PubMed  Google Scholar 

  74. Ro HS, Lee NJ, Lee CW, Lee HS (2006) Isolation of a novel mycovirus OMIV in Pleurotus ostreatus and its detection using a triple antibody sandwich-ELISA. J Virol Methods 138(1):24–29. https://doi.org/10.1016/j.jviromet.2006.07.016

    CAS  Article  PubMed  Google Scholar 

  75. Song HY, Choi HJ, Jeong H, Choi D, Kim JM (2016) Viral effects of a dsRNA mycovirus (PoV-ASI2792) on the vegetative growth of the edible mushroom Pleurotus ostreatus. Mycobiology 44(4):283–290. https://doi.org/10.5941/MYCO.2016.44.4.283

    Article  PubMed  PubMed Central  Google Scholar 

  76. Qiu LY, Li YP, Liu YM, Gao YQ, Qi YC, Shen JW (2010) Particle and naked RNA mycoviruses in industrially cultivated mushroom Pleurotus ostreatus in China. Fungal Biol 114(5):507–513. https://doi.org/10.1016/j.funbio.2010.04.001

    CAS  Article  PubMed  Google Scholar 

  77. Lim WS, Jeong JH, Jeong RD, Yoo YB, Yie SW, Kim KH (2005) Complete nucleotide sequence and genome organization of a dsRNA partitivirus infecting Pleurotus ostreatus. Virus Res 108(1):111–119. https://doi.org/10.1016/j.virusres.2004.08.017

    CAS  Article  PubMed  Google Scholar 

  78. Ushiyama R, Nakai Y, Ikegami M (1977) Evidence for double-stranded RNA from polyhedral virus-like particles in Lentinus edodes (Berk.) Sing. Virology 77(2):880–883. https://doi.org/10.1016/0042-6822(77)90512-8

    CAS  Article  PubMed  Google Scholar 

  79. Shen XR, Chen MJ, Shen JY, Pan YJ, Gong ZX (1993) The detection of single-stranded RNA in an isometric virus-like particle from Shiitake mushroom [Lentinus edodes (Berk.) Sing.]. Ann Appl Biol 122(2):271–277. https://doi.org/10.1111/j.1744-7348.1993.tb04032.x

    Article  Google Scholar 

  80. Rytter JL, Royse DJ, Romaine CP (1991) Incidence and diversity of double-stranded RNA in Lentinula edodes. Mycologia 83(4):506–510. https://doi.org/10.1080/00275514.1991.12026041

    CAS  Article  Google Scholar 

  81. Ushiyama R, Nakai Y (1980) Intracellular virus-like particles in Lentinus edodes. J Gen Virol 46(2):507–509. https://doi.org/10.1099/0022-1317-46-2-507

    Article  Google Scholar 

  82. Magae Y, Hayashi N (1999) Double-stranded RNA and virus-like particles in the edible basidiomycete Flammulina velutipes (Enokitake). FEMS Microbiol Lett 180(2):331–335. https://doi.org/10.1016/S0378-1097(99)00503-0

    CAS  Article  PubMed  Google Scholar 

  83. Magae Y, Sunagawa M (2010) Characterization of a mycovirus associated with the brown discoloration of edible mushroom, Flammulina velutipes. Virol J 7:342. https://doi.org/10.1186/1743-422X-7-342

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  84. Komatsu A, Kondo H, Sato M, Kurahashi A, Nishibori K, Suzuki N, Fujimori F (2019) Isolation and characterization of a novel mycovirus infecting an edible mushroom, Grifola frondosa. Mycoscience 60(4):211–220. https://doi.org/10.1016/j.myc.2019.01.005

    Article  Google Scholar 

  85. Sahin E, Keskin E, Akata I (2021) Novel and diverse mycoviruses co-inhabiting the hypogeous ectomycorrhizal fungus Picoa juniperi. Virology 552:10–19. https://doi.org/10.1016/j.virol.2020.09.009

    CAS  Article  PubMed  Google Scholar 

  86. Sahin E, Keskin E, Akata I (2021) The unique genome organization of two novel fusariviruses hosted by the true morel mushroom Morchella esculenta. Virus Res 302:198486. https://doi.org/10.1016/j.virusres.2021.198486

    CAS  Article  PubMed  Google Scholar 

  87. Li XF, Xie JT, Hai D, Sui KP, Yin WQ, Sossah FL, Jiang DH, Song B, Li Y (2020) Molecular characteristics of a novel ssRNA virus isolated from Auricularia heimuer in China. Arch Virol 165(6):1495–1499. https://doi.org/10.1007/s00705-020-04615-5

    CAS  Article  PubMed  Google Scholar 

  88. Li XF, Sui KP, Xie JT, Hai D, Yin WQ, Sossah FL, Jiang DH, Song B, Li Y (2020) Molecular characterization of a novel fusarivirus infecting the edible fungus Auricularia heimuer. Arch Virol 165(11):2689–2693. https://doi.org/10.1007/s00705-020-04781-6

    CAS  Article  PubMed  Google Scholar 

  89. Voth PD, Mairura L, Lockhart BE, May G (2006) Phylogeography of Ustilago maydis virus H1 in the USA and Mexico. J Gen Virol 87(11):3433–3441. https://doi.org/10.1099/vir.0.82149-0

    CAS  Article  PubMed  Google Scholar 

  90. Honda S, Eusebio-Cope A, Miyashita S, Yokoyama A, Aulia A, Shahi S, Kondo H, Suzuki N (2020) Establishment of Neurospora crassa as a model organism for fungal virology. Nat Commun 11(1):5627. https://doi.org/10.1038/s41467-020-19355-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  91. Kim SW, Kim MG, Jung HA, Lee KH, Lee HS, Ro HS (2008) An application of protein microarray in the screening of monoclonal antibodies against the oyster mushroom spherical virus. Anal Biochem 374(2):313–317. https://doi.org/10.1016/j.ab.2007.12.010

    CAS  Article  PubMed  Google Scholar 

  92. Kim SW, Kim MG, Kim J, Lee HS, Ro HS (2008) Detection of the mycovirus OMSV in the edible mushroom, Pleurotus ostreatus, using an SPR biosensor chip. J Virol Methods 148(1):120–124. https://doi.org/10.1016/j.jviromet.2007.10.025

    CAS  Article  PubMed  Google Scholar 

  93. Revill PA, Wright PJ (1997) RT-PCR detection of dsRNAs associated with La France disease of the cultivated mushroom Agaricus bisporus (Lange) Imbach. J Virol Methods 63(1):17–26. https://doi.org/10.1016/S0166-0934(96)02113-1

    CAS  Article  PubMed  Google Scholar 

  94. Romaine CP, Schlagnhaufer B (1995) PCR analysis of the viral complex associated with La France disease of Agaricus bisporus. Appl Environ Microbiol 61(6):2322–2325. https://doi.org/10.1128/aem.61.6.2322-2325.1995

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  95. Kim JM, Song HY, Choi HJ, Yun SH, So KK, Ko HK, Kim DH (2015) Changes in the mycovirus (LeV) titer and viral effect on the vegetative growth of the edible mushroom Lentinula edodes. Virus Res 197:8–12. https://doi.org/10.1016/j.virusres.2014.11.016

    CAS  Article  PubMed  Google Scholar 

  96. Urayama S, Katoh Y, Fukuhara T, Arie T, Moriyama H, Teraoka T (2015) Rapid detection of Magnaporthe oryzae chrysovirus 1-A from fungal colonies on agar plates and lesions of rice blast. J Gen Plant Pathol 81(2):97–102. https://doi.org/10.1007/s10327-014-0567-6

    Article  Google Scholar 

  97. Zhang YZ, Chen YM, Wang W, Qin XC, Holmes EC (2019) Expanding the RNA virosphere by unbiased metagenomics. Annu Rev Virol 6(1):119–139. https://doi.org/10.1146/annurev-virology-092818-015851

    CAS  Article  PubMed  Google Scholar 

  98. Wang J, Ni YX, Liu XT, Zhao H, Xiao YN, Xiao XQ, Li SJ, Liu HY (2020) Divergent RNA viruses in Macrophomina phaseolina exhibit potential as virocontrol agents. Virus Evol 7(1):veaa95. https://doi.org/10.1093/ve/veaa095

    Article  Google Scholar 

  99. Sutela S, Forgia M, Vainio EJ, Chiapello M, Daghino S, Vallino M, Martino E, Girlanda M, Perotto S, Turina M (2020) The virome from a collection of endomycorrhizal fungi reveals new viral taxa with unprecedented genome organization. Virus Evol 6(2):veaa76. https://doi.org/10.1093/ve/veaa076

    Article  Google Scholar 

  100. Jia JC, Fu YP, Jiang DH, Mu F, Cheng JS, Lin Y, Li B, Marzano SL, Lee Y, Xie JT (2021) Interannual dynamics, diversity and evolution of the virome in Sclerotinia sclerotiorum from a single crop field. Virus Evol 7(1):veab032. https://doi.org/10.1093/ve/veab032

    Article  PubMed  PubMed Central  Google Scholar 

  101. Ruiz-Padilla A, Rodríguez-Romero J, Gómez-Cid I, Pacifico D, Ayllón MA, Wickner RB (2021) Novel mycoviruses discovered in the mycovirome of a necrotrophic fungus. MBio 12(3):e03705. https://doi.org/10.1128/mBio.03705-20

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  102. Rumbou A, Vainio EJ, Büttner C (2021) Towards the forest virome: high-throughput sequencing drastically expands our understanding on virosphere in temperate forest ecosystems. Microorganisms 9(8):1730

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  103. Marzano SL, Domier LL (2016) Reprint of “Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes.” Virus Res 219:11–21. https://doi.org/10.1016/j.virusres.2016.05.012

    CAS  Article  PubMed  Google Scholar 

  104. Myers JM, Bonds AE, Clemons RA, Thapa NA, Simmons DR, Carter-House D, Ortanez J, Liu P, Miralles-Durán A, Desirò A, Longcore JE, Bonito G, Stajich JE, Spatafora JW, Chang Y, Corrochano LM, Gryganskyi A, Grigoriev IV, James TY, Taylor JW (2020) Survey of early-diverging lineages of fungi reveals abundant and diverse mycoviruses. MBio 11(5):e02027. https://doi.org/10.1128/mBio.02027-20

    Article  PubMed  PubMed Central  Google Scholar 

  105. 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(7):e0219207. https://doi.org/10.1371/journal.pone.0219207

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  106. Kaminski MM, Abudayyeh OO, Gootenberg JS, Zhang F, Collins JJ (2021) CRISPR-based diagnostics. Nat Biomed Eng 5(7):643–656. https://doi.org/10.1038/s41551-021-00760-7

    CAS  Article  PubMed  Google Scholar 

  107. Wang X, Shang X, Huang X (2020) Next-generation pathogen diagnosis with CRISPR/Cas-based detection methods. Emerg Microbes Infect 9(1):1682–1691. https://doi.org/10.1080/22221751.2020.1793689

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  108. Sharma SK, Gupta OP, Pathaw N, Sharma D, Maibam A, Sharma P, Sanasam J, Karkute SG, Kumar S, Bhattacharjee B (2021) CRISPR-Cas-Led revolution in diagnosis and management of emerging plant viruses: new avenues toward food and nutritional security. Front Nutr 8:751512. https://doi.org/10.3389/fnut.2021.751512

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  109. Zhang CH, Liu YM, Qi YC, Gao YQ, Shen JW, Qiu LY (2010) Comparisons of different methods for virus-elimination of edible fungi. Chin J Virol 26(3):249–254

    Google Scholar 

  110. Kwon YC, Jeong DW, Gim SI, Ro HS, Lee HS (2012) Curing viruses in Pleurotus ostreatus by growth on a limited nutrient medium containing cAMP and rifamycin. J Virol Methods 185(1):156–159. https://doi.org/10.1016/j.jviromet.2012.06.002

    CAS  Article  PubMed  Google Scholar 

  111. Sun YJ, Guo MP, Wang JJ, Bian YB, Xu ZY (2022) Curing two predominant viruses occurring in Lentinula edodes by chemotherapy and mycelial fragmentation methods. J Virol Methods 300:114370. https://doi.org/10.1016/j.jviromet.2021.114370

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by China Postdoctoral Science Foundation (2017M621223), Scientific and Technological Developing Project of Jilin Province (20210204047YY), and 111 Project (D17014).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

This article does not contain any experiments involving human participants or animals.

Additional information

Edited by Zhen F. Fu.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 222 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Gao, J. & Li, Y. Diversity of mycoviruses in edible fungi. Virus Genes (2022). https://doi.org/10.1007/s11262-022-01908-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11262-022-01908-6

Keywords

  • Mycovirus
  • Edible fungi
  • Diversity
  • Evolution