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Mycovirology (Ghabrial&Suzuki, 2009) [1] is the study of viruses infecting fungi, also called mycoviruses. It is a special subdivision of the general field of virology and describes taxonomy, host range, origin and evolution, transmission and movement of mycoviruses and their impact on host phenotype.

Mycovirus taxonomy

The majority of mycoviruses have double stranded RNA (dsRNA) genomes and isometric particles, but approximately 30 % have positive single stranded RNA (ssRNA) genomes (Pearson et al., 2009[2]; Bozarth et al., 1972[3]). So far there is only one true example of a ssDNA mycovirus. A geminivirus-related virus was found in Sclerotinia sclerotiorum conferring hypovirulence to its host (Yu et al., 2010[4]). The updated 9th ICTV report on virus taxonomy (King et al., 2011)[5] lists over 90 mycovirus species covering 10 viral families, of which 20 % were unassigned to a genus or sometimes not even to a family. Isometric forms predominate mycoviral morphologies in comparison to rigid rods, flexuous rods, clubshaped particles, enveloped bacilliform particles, and Herpesvirus-like viruses (Varga et al., 2003)[6]. The lack of genomic data often hampers a conclusive assignment to already established groups of viruses or makes it impossible to erect new families and genera. The latter is true for many unencapsidated dsRNA viruses, which are assumed to be viral, but missing sequence data prevented their classification so far (Pearson et al., 2009)[2]). So far, viruses of the families Partitiviridae, Totiviridae, and Narnavriridae are dominating the ‘mycovirus sphere’.

Listing of all formally named and recognised mycoviruses summarised from “Virus Taxonomy: The Ninth Report of the International Committee on Taxonomy of Viruses” (King et al., 2011).

Host range and incidence

Mycoviruses are common in fungi (Herrero et al., 2009) and are found in all four phyla of the true fungi: Chytridiomycota, Zygomycota, Ascomycota and Basidiomycota. Fungi are commonly infected with two or more unrelated viruses and also with defective dsRNA and/or satellite dsRNA (Ghabrial et al., 2008[1]; Howitt et al., 2006[7]). There also viruses, which use fungi only as vectors and are distinct from mycoviruses, because they cannot reproduce in the fungal cytoplasm (Adams, 1991[8]). It is generally assumed that the natural host range of mycoviruses is confined to closely related vegetability compatibility groups that allow for cytoplasmic fusion (Buck, 1986[9]), but some mycoviruses can replicate in taxonomically different fungal hosts (Ghabrial et al., 2009 (Suppl. Section 1)[10]). Good examples are mitoviruses found in the two fungal species Sclerotinia homoeocarpa and Ophiostoma novo-ulmi (Deng et al., 2003[11]). Furthermore, Nuss et al. (2005) described that it is possible to extend the natural host range of Cryphonectria parasitica hypovirus 1 (CHV1) to several fungal species that are closely related to Cryphonectria parasitica using in vitro virus transfection techniques (Chen et al., 1994[12]). CHV1 can also propagate in the genera Endothia and Valsa (Ghabrial et al., 2008[1]), which belong to the two distinct families Cryphonectriaceae and Diaporthaceae, respectively.

Origin and evolution

DsRNA as well as ssRNA are assumed to be very ancient and presumably originated from the ‘RNA world’ as both types of RNA viruses infect bacteria as well as eukaryotes (Forterre, 2006)[13]. Although the origin of viruses is still not well understood, Koonin (2008)[14] recently presented data which suggest that viruses invaded the emerging ‘supergroups’ of eukaryotes from an ancestral pool in a very early stage of life on earth. According to Koonin[14], RNA viruses colonized eukaryotes first and subsequently co-evolved with their hosts. This concept fits well with the proposed ‘ancient co-evolution hypothesis’, which also assumes a long co-evolution of viruses and fungi (Varga, 2003[6]; Pearson et al., 2009[2]). ‘The ancient coevolution hypothesis’ could contribute some explanation why mycoviruses are so diverse (Varga, 2003[6]. Dawe&Nuss (2001)[15] also suggested that it is very likely that plant viruses containing a movement protein have evolved from mycoviruses by introducing of an extracellular phase into their life cycle, rather than eliminating it. Furthermore, the recent discovery of an ssDNA mycovirus tempted Yu et al. (2010)[4] to suggest that RNA and DNA viruses might have common evolutionary mechanisms. However, there are many cases, where mycoviruses grouped together with plant viruses. For example CHV1 showed phylogenetic relatedness to the ssRNA genus Potyvirus (Fauquet et al., 2005)[16] and some ssRNA viruses, which were assumed to confer hypovirulence or debilitation, were often found to be more closely related to plant viruses than to other mycoviruses (Pearson et al., 2009[2])). Therefore, another theory arose that these viruses moved from a plant host to plant pathogenic fungal host or vice versa. This ‘plant virus hypothesis’ may not explain how mycoviruses developed originally, but it could help to understand how they evolved further.

Transmission of mycoviruses

A significant difference between the genomes of mycoviruses to other viruses is the absence of genes for ‘cell-to-cell movement’ proteins. It is therefore assumed that mycoviruses only move intercellularly during cell division (e.g. sporogenesis) or via hyphal fusion (Ghabrial et al., 1994[17]; 2008[1]). Mycoviruses might simply not need an external route of infection as they have many means of transmission and spread due to their fungal host’s life style:

  • Plasmogamy and cytoplasmic exchange over extended periods of time
  • Production of vast amounts of asexual spores
  • Overwintering via sclerotia (Liu, 2009[18])
  • More or less effective transmission into sexual spores

However, there are potential barriers to mycovirus spread due to vegetative incompatibility and variable transmission to sexual spores. Transmission to sexually produced spores can range from 0% to 100 % depending on the virus-host combination (Ghabrial et al., 2008[1]). Transmission between species of the same genus sharing the same habitat has also been reported including Cryphonectria (C. parasitica and C. sp), Sclerotinia (S. sclerotium and S. minor), and Ophistoma (O. ulmi and O. novo-ulmi) (Liu et al., 2003[19]; Melzer et al., 2005[20]). Intraspecies transmission was also reported by van Diepeningen et al. (2000)[21] between Fusarium poae and black Aspergillus isolates. However, it is not known how fungi overcome the genetic barrier; whether there is some form of recognition process during physical contact or some other means of exchange, such as vectors. Studies by van Diepeningen (2006)[22] using Aspergillus sp. indicated that transmission efficiencies might depend on the hosts viral infection status (infected with no, different, or same virus), and that mycoviruses might play a role in the regulation of secondary mycoviral infection. Whether this is also true for other fungi is not yet known. In contrast to acquiring mycoviruses spontaneously, the loss of mycoviruses seems very infrequent (Van Diepeningen, 2006[22]) and suggests that either viruses actively moved into spores and new hyphal tips, or the fungus might facilitate the mycoviral transport in some other way.

Movement of mycoviruses within fungi

Although it is not known yet whether viral transport is an active or passive process, it is generally assumed that fungal viruses move forward by plasma streaming (Sasaki et al., 2006[23]). Theoretically they could drift with the cytoplasm as it extends into new hyphae, or attach to the web of microtubuli, which would drag them through the internal cytoplasmic space. That might explain how they pass through septa and bypass woronin bodies. However, some researchers have found them located next to septum walls (Vilches & Castillo, 1997[24]; Bozarth, 1972[3]), which could imply that they ‘got stuck’ and were not able to move actively forward themselves. Others suggested that the transmission of viral mitochondrial dsRNA may play an important role in the movement of mitoviruses found in B. cinerea (Wu et al., 2010[25]).

Impact on host phenotype

Phenotypic effects of mycoviral infections can vary from advantageous to deleterious, but most of them are symptomless or cryptic. The connection between phenotype and mycovirus presence is not always straight forward. Several reasons may account for this. First, the lack of appropriate infectivity assays often hindered the researcher from reaching a coherent conclusion (McCabe et al., 1999[26]). Secondly, mixed infection or unknown numbers of infecting viruses make it very difficult to associate a particular phenotypic change with the investigated virus. Although most mycoviruses often do not seem to disturb their host’s fitness, this does not necessarily mean they are living unrecognized by their hosts. As described by May&Nowak (1995)[27] and Araújo et al. (2003)[28] a neutral co-existence might just be the result of a long co-evolutionary process. Accordingly, symptoms may only appear when certain conditions of the virus-fungus-system change and get out of balance. This could be external (environmental) as well as internal (cytoplasmic). It is not known yet why some mycoviruses-fungus-combinations are typically detrimental while others are symptomless or even beneficial. Nevertheless, harmful effects of mycoviruses are economically interesting, especially if the fungal host is a phytopathogen and the mycovirus could be exploited as biocontrol agent. The best example is represented by the case of CHV1 and C. parasitica (Ghabrial et al., 2008[1]). Other examples of deleterious effects of mycoviruses are the ‘La France’ disease of Agaricus biporus (Hollings, 1962[29]; Ro et al., 2006[30]) and the mushroom diseases caused by Oyster mushroom spherical virus (Yu et al., 2003[31]) and Oyster mushroom isometric virus (Ro et al., 2006[30]).


In summary, the main negative effects of mycoviruses are:

  • Decreased growth rate (Moleleki et al., 2003[32])
  • Lack of sporulation (Moleleki et al., 2003[32])
  • Attenuation of virulence (Suzaki et al., 2005[33])
  • Reduced germination of basidiospores (Ihrmark et al., 2004[34])


Hypovirulent phenotypes do not appear to correlate with specific genome features and it seems there is not one particular metabolic pathway causing hypovirulence but several (Xie et al., 2006[35]). In addition to negative effects, beneficial interactions do also occur. Well described examples are the killer phenotypes in yeasts (Schmitt et al., 2002[36]) and Ustilago (Marquina et al., 2002[37]). Killer isolates secrete proteins that are toxic to sensitive cells of the same or closely related species while the producing cells themselves are immune. Most of these toxins degrade the cell membrane (Schmitt et al., 2002[36]). There are potentially interesting applications of killer isolates in medicine, food industry, and agriculture (Schmitt et al., 2002[36]; Dawe&Nuss, 2001[15]). And Marquez et al. (2007)[38] who describe a three-part system involving a mycovirus of an endophytic fungus (Curvularia protuberata) of the grass Dichanthelium lanuginosum, which provides a thermal tolerance to the plant, enabling it to inhabit adverse environmental niches.

References

  1. ^ a b c d e f Ghabrial, S. A., Suzuki, N. (2009). Viruses of Plant Pathogenic Fungi. Annual Review of Phytopathology, 47 (1): 353-384.
  2. ^ a b c d Pearson, M. N., Beever, R. E., Boine, B., Arthur, K. (2009). Mycoviruses of filamentous fungi and their relevance to plant pathology. Molecular Plant Pathology, 10 (1): 115-128.
  3. ^ a b Bozarth, R.F., Mycoviruses: a new dimension in microbiology. Environmental Health Perspectives, 1972: p. 23-39
  4. ^ a b Yu, X., Li, B., Fu, Y., Jiang, D., Ghabrial, S. A., Li, G., Peng, Y., Xie, J., Cheng, J., Huang, J., Yi, X. (2010). A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proceedings of the National Academy of Sciences of the United States of America, 107 (18): 8387-8392.
  5. ^ [1], King, A. M. Q., Lefkowitz E. M., Adams, J., Carstens, E. B. (2011). Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses (ICTV). San Diego, CA: Elsevier Academic.
  6. ^ a b c Varga, J., Toth, B., and Vagvolgyi, C. (2003). Recent Advances in Mycovirus research. Acta Microbiologica et Immunologica Hungrica, 50 (1): 77-94.
  7. ^ Howitt, R., Beever, R., Pearson, M. N., Forster, R. L. S. (2006). Genome characterization of a flexuous rod-shaped mycovirus, Botrytis virus X, reveals high amino acid identity to genes from plant potex-like viruses. Archives of Virology, 151 (3): 563-579.
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  11. ^ Deng, F., Xu, R., and Boland, G. J. (2003). Hypovirulence-Associated Double-Stranded RNA from Sclerotinia homoeocarpa Is Conspecific with Ophiostoma novo-ulmi Mitovirus 3a-Ld. Phytopathology, 93 (11): 1407-14.
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  19. ^ Liu, Y. C., Linder-Basso, D., Hillman, B. I., Kaneko, S., Milgroom, M. G. (2003). Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria. Molecular Ecology, 12 (6): 1619-1628.
  20. ^ Melzer, M. S., Deng, F., Boland, G. J. (2005). Asymptomatic infection, and distribution of Ophiostoma mitovirus 3a (OMV3a), in populations of Sclerotinia homoeocarpa. Canadian Journal of Plant Pathology, 27 (4:, 610-615.
  21. ^ Van Diepeningen, A. D., Debets, A. J. M., Slakhorst, S. M., Fekete, C., Hornok, L., Hoekstra, R. F. (2000). Interspecies virus transfer via protoplast fusions between Fusarium poae and black Aspergillus strains. Fungal Genetics Newsletter, 47: 99-100.
  22. ^ a b Van Diepeningen, A. D., Debets, A., and Hoekstra, R. (2006). Dynamics of dsRNA mycoviruses in black Aspergillus populations. Fungal Genetics and Biology, 43: 446-452.
  23. ^ Sasaki, A., Kanematsu, S., Onoue, M., Oyama, Y., Yoshida, K. (2006). Infection of Rosellinia necatrix with purified viral particles of a member of Partitiviridae (RnPV1-W8). Archives of Virology, 151 (4): 697-707.
  24. ^ Vilches, S.&Castillo, A. (1997). A double-stranded RNA mycovirus in Botrytis cinerea, FEMS Microbiology Letters, 155 (1): 125-130.
  25. ^ Wu, M. D., Zhang, L., Li, G., Jiang, D., Ghabrial, S. A. (2010). Genome characterization of a debilitation-associated mitovirus infecting the phytopathogenic fungus Botrytis cinerea. Virology,406 (1): 117-126.
  26. ^ McCabe, P. M., Pfeiffer, P., and Van Alfen, N. K. (1999). The influence of dsRNA viruses on the biology of plant pathogenic fungi. Trends in Microbiology, 7 (9): 377-381.
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  29. ^ Hollings, M. (1962). Viruses associated with dieback disease of cultivated mushrooms. Nature, 196: 962-965.
  30. ^ a b Ro, H. S., Lee, N. J., Lee, C. W., Lee, H. S. (2006). Isolation of a novel mycovirus OMIV in Pleurotus ostreatus and its detection using a triple antibody sandwich-ELISA. Journal of Virological Methods, 138 (1-2): 24-29.
  31. ^ Yu, H. J., Lim, D., and Lee, H. S. (2003). Characterization of a novel single-stranded RNA mycovirus in Pleurotus ostreatus. Virology, 314 (1): 9-15.
  32. ^ a b Moleleki, N., Van Heerden, S. W., Wingfield, M. J., Wingfield, B. D., Preisig, O. (2003). Transfection of Diaporthe perjuncta with Diaporthe RNA virus. Applied and Environmental Microbiology, 69 (7): 3952-3956.
  33. ^ Suzaki, K., Ikeda, K. I., Sasaki, A., Kanematsu, S., Matsumoto, N., Yoshida, K. (2005). Horizontal transmission and host-virulence attenuation of totivirus in violet root rot fungus Helicobasidium mompa. Journal of General Plant Pathology, 71 (3): 161-68.
  34. ^ Ihrmark, K., Stenström, E., and Stenlid, J. (2004). Double-stranded RNA transmission through basidiospores of Heterobasidion annosum. Mycological Research, 108 (2): 149-153.
  35. ^ Xie, J., Wei, D., Jiang, D., Fu, Y., Li, G., Ghabrial, S., Peng, Y. (2006). Characterization of debilitation-associated mycovirus infecting the plant-pathogenic fungus Sclerotina sclerotorium. Journal of General Virology, 87 (1): 241-249.
  36. ^ a b c Schmitt, M. J. and Breinig, F. (2002). The viral killer system in yeast: From molecular biology to application. FEMS Microbiology Reviews, 26 (3): 257-276.
  37. ^ Marquina, D., Santos, A., Peinado, J. (2002). Biology of killer yeasts. International Microbiology, 5 (2): 65-71.
  38. ^ Márquez, L. M., Redman, R. S., Rodriguez, R. J., Roossinck, M. J. (2007). A Virus in a Fungus in a Plant: Three-Way Symbiosis Required for Thermal Tolerance. Science, 315 (5811): 513-15.
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