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Mycoviruses are [[viruses]] that infect [[fungi]]. They have been identified in all major fungal families. Most identified so far have had double stranded [[RNA]] [[genomes]], often with more than one dsRNA present per virus particle, and have been spherical in shape.<ref>Bozarth, R.F., Mycoviruses: a new dimension in microbiology. Environmental Health Perspectives, 1972: p. 23-39</ref> To be a true mycovirus, they must demonstrate an ability to be transmitted - in other words be able to infect other healthy fungi. Many double stranded RNA elements that have been described in fungi do not fit this description, and in these cases they are referred to as virus like particles or [[VLP]]s.
Mycoviruses (ancient Greek μύκης mykes: fungus and latin [[virus]])are [[viruses]] that infect [[fungi]]. 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<ref name="Pearson">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.</ref>; Bozarth et al., 1972<ref name="Boz">Bozarth, R.F., Mycoviruses: a new dimension in microbiology. Environmental Health Perspectives, 1972: p. 23-39</ref>). To be a true mycovirus, they must demonstrate an ability to be transmitted - in other words be able to infect other healthy fungi. Many double stranded RNA elements that have been described in fungi do not fit this description, and in these cases they are referred to as virus like particles or [[VLP]]s. Preliminary results indicate that most mycoviruses codiverge with their hosts, i.e. their [[phylogeny]] is largely congruent with the one of their hosts<ref>

Preliminary results indicate that most mycoviruses codiverge with their hosts, i.e. their [[phylogeny]] is largely congruent with the one of their hosts<ref>
{{Citation
{{Citation
| last = Göker
| last = Göker
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</ref>. However, many virus families containing mycoviruses have only sparsely been sampled.
</ref>. However, many virus families containing mycoviruses have only sparsely been sampled.


== La France Disease ==
== Mycovirology ==


Mycovirology (Ghabrial&Suzuki, 2009) <ref name= "Ghabrial">Ghabrial, S. A., Suzuki, N. (2009). Viruses of Plant Pathogenic Fungi. Annual Review of Phytopathology, 47 (1): 353-384.</ref> is the study of viruses infecting fungi, also called [[mycovirus]]es. It is a special subdivision of the general field of [[virology]] and describes taxonomy, host range, origin and evolution, transmission and movement of [[mycovirus]]es and their impact on host phenotype.
⚫
An example of a true mycovirus is the causal agent of La France disease. This is a disease that affects the edible [[mushroom]], [[Agaricus bisporus]]. It is also known as X disease, watery stripe, dieback and brown disease. [[Symptoms]] include:

⚫
== History ==

The first record of an economic impact of mycoviruses on fungi was recorded by cultivated mushrooms (''[[Agaricus bisporus]]'') in the late 1940’s and was called the La France disease (Hollings, 1962)<ref name="Hollings" >Hollings, M. (1962). Viruses associated with dieback disease of cultivated mushrooms. Nature, 196: 962-965.</ref>. Hollings found more than three different types of viruses in the abnormal sporophores. This report marks the beginning of [[mycovirology]] (Ghabrial et al., 2008) <ref>Ghabrial, S. A., Suzuki, N. (2008). Fungal Viruses. In B. W. J. Mahy and M. H. V. Van Regenmortel (ed.), Encyclopedia of Virology, 3rd ed., vol. 2. Elsevier, Oxford, United Kingdom. p. 284-291.</ref>.

⚫
The La France Disease is also known as X disease, watery stripe, dieback and brown disease. [[Symptoms]] include:


* Reduced [[Crop yield|yield]]
* Reduced [[Crop yield|yield]]
* Slow and aberrant [[mycelial]] growth
* Slow and aberrant [[mycelial]] growth
* Waterlogging of tissue
* [[malformation]]
* [[malformation]]
* Premature maturation
* Premature maturation
Line 37: Line 42:
Mushrooms have shown no resistance to the virus, and so control has had to be via [[hygenic]] practises to stop the spread of the virus.
Mushrooms have shown no resistance to the virus, and so control has had to be via [[hygenic]] practises to stop the spread of the virus.


However, the best known mycovirus is ''[[Cryphonectria parasitica]]'' hypovirus 1 (CHV1). CHV1 is exceptional amongst mycoviral research due its success as biocontrol agent against chestnut blight in Europe, but also because it is a model organism for studying hypovirulence in fungi. However, this system is only being used in Europe routinely, because of the relative small number of vegetative compatibility groups (VCGs) on this continent. In contrast, in North America the distribution of the hypovirulent phenotype is often prevented because fungal hyphae cannot fuse and exchange their cytoplasmic content due to an incompatibility reaction. In the United States of America at least 35 VCGs were found (Anagnostakis, 1998)<ref name=Anagnostakis >Anagnostakis, S. L., Chen, B., Geletka, L. M., Nuss, D. L. (1998). Hypovirus Transmission to Ascospore Progeny by Field-Released Transgenic Hypovirulent Strains of ''Cryphonectria parasitica''. Phytopathology, 88 (7); 598-604."</ref>. A similar situation seems to be present in China and Japan where 71 VCGs were identified so far (Liu&Milgroom, 2007)<ref name=Liu&Milgroom >Liu Y. J., Milgroom, M.G. (2007). High diversity of vegetative compatibility types in ''Cryphonectria parasitica'' in Japan and China. Mycologia, 99, 279–284."</ref> .
⚫
== Notes ==

== 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<ref name="Pearson" />; Bozarth et al., 1972<ref name="Boz" />). 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<ref name= "Yu">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.</ref>). The updated 9th ICTV report on virus taxonomy (King et al., 2011)<ref>[http://www.ictvonline.org], 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.</ref> 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)<ref name="Varga">Varga, J., Toth, B., and Vagvolgyi, C. (2003). Recent Advances in Mycovirus research. Acta Microbiologica et Immunologica Hungrica, 50 (1): 77-94.</ref>. 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)<ref name="Pearson" />). So far, viruses of the families ''[[Partitiviridae]]'', ''[[Totiviridae]]'', and ''Narnavriridae'' are dominating the ‘mycovirus sphere’.

[[file:Listing of all formally named and recognised mycoviruses.png|thumb|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<ref name="Ghabrial" />; Howitt et al., 2006<ref>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.</ref>). There also viruses, which use fungi only as vectors and are distinct from mycoviruses, because they cannot reproduce in the fungal cytoplasm (Adams, 1991<ref>Adams, M. J. (1991). 'Transmission of plant viruses by fungi', Annals of Applied Biology, 118 (2): 479-92.</ref>). 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<ref>Buck, K. W. (1986). Fungal Virology- An overview', in K. Buck (ed.), Fungal Virology (Boca Raton: CRC Press): 1-84.</ref>), but some mycoviruses can replicate in taxonomically different fungal hosts (Ghabrial et al., 2009 (Suppl. Section 1)<ref name="Ghabrial" />). Good examples are mitoviruses found in the two fungal species ''Sclerotinia homoeocarpa'' and ''Ophiostoma novo-ulmi'' (Deng et al., 2003<ref>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.</ref>). 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<ref>Chen, B., Choi, G. H., and Nuss, D. L. (1994). Attenuation of fungal virulence by synthetic infectious hypovirus transcripts. Science, 264 (5166): 1762-1764.</ref>). CHV1 can also propagate in the genera ''Endothia'' and ''Valsa'' (Ghabrial et al., 2008<ref name="Ghabrial" />), 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)<ref>Forterre, P. (2006). The origin of viruses and their possible roles in major evolutionary transitions. Virus Research, 117 (1): 5-16.</ref>. Although the origin of viruses is still not well understood, Koonin (2008)<ref name="Koonin">Koonin, E. V. and Wolf, Y. I. (2008). Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Research, 36 (21): 6688-6719.</ref> 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<ref name="Koonin" />, 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<ref name="Varga" />; Pearson et al., 2009<ref name="Pearson" />). ‘The ancient coevolution hypothesis’ could contribute some explanation why mycoviruses are so diverse (Varga, 2003<ref name="Varga" />. Dawe&Nuss (2001)<ref name="Dawe">Dawe, A. L., Nuss, D. L. (2001). Hypoviruses and chestnut blight: Exploiting viruses to understand and modulate fungal pathogenesis. Annual Review of Genetics, 35: 1-29.</ref> 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)<ref name="Yu" /> 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)<ref>Fauquet, C. M., Mayo, M. A., Maniloff, J. (2005). Virus Taxonomy: Classification and Nomenclature of Viruses: The Eighth Report of the International Committee on the Taxonomy of Viruses. San Diego, CA: Elsevier Academic.</ref> 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<ref name="Pearson" />)). 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 ==

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<ref>Ghabrial, S. A. (1994). New Developments in Fungal Virology. In Frederick A. Murphy Karl Maramorosch and J. Shatkin Aaron (eds.), Advances in Virus Research (Volume 43: Academic Press): 303-388.</ref>; 2008<ref name="Ghabrial" />). 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<ref>Liu, H., Fu, Y., Jiang, D., Li, G., Xie, J., Peng, Y., Yi, X., Ghabrial, S. A. (2009). A novel mycovirus that is related to the human pathogen Hepatitis E virus and rubi-like viruses. Journal of Virology, 83 (4): 1981-1991. Phytopathology, 155 (2): 65-69.</ref>)
* 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<ref name="Ghabrial" />). 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<ref>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.</ref>; Melzer et al., 2005<ref>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.</ref>). Intraspecies transmission was also reported by van Diepeningen et al. (2000)<ref>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.</ref> 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)<ref name="Diep">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.</ref> 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<ref name="Diep" />) 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<ref>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.</ref>). 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<ref>Vilches, S.&Castillo, A. (1997). A double-stranded RNA mycovirus in ''Botrytis cinerea'', FEMS Microbiology Letters, 155 (1): 125-130.</ref>; Bozarth, 1972<ref name="Boz" />), 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<ref>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.</ref>).

== 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<ref>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.</ref>). 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)<ref>May, R. M., Nowak, M. A. (1995). Coinfection and the Evolution of Parasite Virulence. Proceedings: Biological Sciences, 261 (1361): 209-215.</ref> and Araújo et al. (2003)<ref>Araújo, A., Jansen, A. M., Bouchet, F., Reinhard, K., Ferreira, L. F. (2003). Parasitism, the Diversity of Life, and Paleoparasitology. Memorias do Instituto Oswaldo Cruz, 98 (SUPPL. 1): 5-11.</ref> 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<ref name="Ghabrial" />). Other examples of deleterious effects of [[mycovirus]]es are the ‘La France’ disease of ''Agaricus biporus'' (Hollings, 1962<ref name="Hollings" />; Ro et al., 2006<ref name="Ro">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.</ref>) and the mushroom diseases caused by Oyster mushroom spherical virus (Yu et al., 2003<ref>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.</ref>) and Oyster mushroom isometric virus (Ro et al., 2006<ref name="Ro" />).


In summary, the main negative effects of mycoviruses are:

* Decreased growth rate (Moleleki et al., 2003<ref name="Mol">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.</ref>)
* Lack of sporulation (Moleleki et al., 2003<ref name="Mol" />)
* Attenuation of virulence (Suzaki et al., 2005<ref>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.</ref>)
* Reduced germination of basidiospores (Ihrmark et al., 2004<ref>Ihrmark, K., Stenström, E., and Stenlid, J. (2004). Double-stranded RNA transmission through basidiospores of Heterobasidion annosum. Mycological Research, 108 (2): 149-153.</ref>)


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<ref>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.</ref>).
In addition to negative effects, beneficial interactions do also occur. Well described examples are the killer phenotypes in yeasts (Schmitt et al., 2002<ref name="Schmitt">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.</ref>) and ''Ustilago'' (Marquina et al., 2002<ref>Marquina, D., Santos, A., Peinado, J. (2002). Biology of killer yeasts. International Microbiology, 5 (2): 65-71.</ref>). 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<ref name="Schmitt" />). There are potentially interesting applications of killer isolates in medicine, food industry, and agriculture (Schmitt et al., 2002<ref name="Schmitt" />; Dawe&Nuss, 2001<ref name="Dawe" />). And Marquez et al. (2007)<ref>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.</ref> 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==


{{Reflist}}
<references/>


[[Category:Viruses]]
[[Category:Viruses]]

Revision as of 15:06, 5 June 2012

Mycoviruses (ancient Greek μύκης mykes: fungus and latin virus)are viruses that infect fungi. 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[1]; Bozarth et al., 1972[2]). To be a true mycovirus, they must demonstrate an ability to be transmitted - in other words be able to infect other healthy fungi. Many double stranded RNA elements that have been described in fungi do not fit this description, and in these cases they are referred to as virus like particles or VLPs. Preliminary results indicate that most mycoviruses codiverge with their hosts, i.e. their phylogeny is largely congruent with the one of their hosts[3]. However, many virus families containing mycoviruses have only sparsely been sampled.

Mycovirology

Mycovirology (Ghabrial&Suzuki, 2009) [4] 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.

History

The first record of an economic impact of mycoviruses on fungi was recorded by cultivated mushrooms (Agaricus bisporus) in the late 1940’s and was called the La France disease (Hollings, 1962)[5]. Hollings found more than three different types of viruses in the abnormal sporophores. This report marks the beginning of mycovirology (Ghabrial et al., 2008) [6].

The La France Disease is also known as X disease, watery stripe, dieback and brown disease. Symptoms include:

  • Reduced yield
  • Slow and aberrant mycelial growth
  • Waterlogging of tissue
  • malformation
  • Premature maturation
  • Increased post-harvest deterioration (reduced shelf life)[7]

Mushrooms have shown no resistance to the virus, and so control has had to be via hygenic practises to stop the spread of the virus.

However, the best known mycovirus is Cryphonectria parasitica hypovirus 1 (CHV1). CHV1 is exceptional amongst mycoviral research due its success as biocontrol agent against chestnut blight in Europe, but also because it is a model organism for studying hypovirulence in fungi. However, this system is only being used in Europe routinely, because of the relative small number of vegetative compatibility groups (VCGs) on this continent. In contrast, in North America the distribution of the hypovirulent phenotype is often prevented because fungal hyphae cannot fuse and exchange their cytoplasmic content due to an incompatibility reaction. In the United States of America at least 35 VCGs were found (Anagnostakis, 1998)[8]. A similar situation seems to be present in China and Japan where 71 VCGs were identified so far (Liu&Milgroom, 2007)[9] .

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[1]; Bozarth et al., 1972[2]). 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[10]). The updated 9th ICTV report on virus taxonomy (King et al., 2011)[11] 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)[12]. 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)[1]). 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[4]; Howitt et al., 2006[13]). There also viruses, which use fungi only as vectors and are distinct from mycoviruses, because they cannot reproduce in the fungal cytoplasm (Adams, 1991[14]). 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[15]), but some mycoviruses can replicate in taxonomically different fungal hosts (Ghabrial et al., 2009 (Suppl. Section 1)[4]). Good examples are mitoviruses found in the two fungal species Sclerotinia homoeocarpa and Ophiostoma novo-ulmi (Deng et al., 2003[16]). 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[17]). CHV1 can also propagate in the genera Endothia and Valsa (Ghabrial et al., 2008[4]), 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)[18]. Although the origin of viruses is still not well understood, Koonin (2008)[19] 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[19], 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[12]; Pearson et al., 2009[1]). ‘The ancient coevolution hypothesis’ could contribute some explanation why mycoviruses are so diverse (Varga, 2003[12]. Dawe&Nuss (2001)[20] 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)[10] 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)[21] 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[1])). 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

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[22]; 2008[4]). 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[23])
  • 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[4]). 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[24]; Melzer et al., 2005[25]). Intraspecies transmission was also reported by van Diepeningen et al. (2000)[26] 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)[27] 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[27]) 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[28]). 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[29]; Bozarth, 1972[2]), 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[30]).

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[31]). 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)[32] and Araújo et al. (2003)[33] 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[4]). Other examples of deleterious effects of mycoviruses are the ‘La France’ disease of Agaricus biporus (Hollings, 1962[5]; Ro et al., 2006[34]) and the mushroom diseases caused by Oyster mushroom spherical virus (Yu et al., 2003[35]) and Oyster mushroom isometric virus (Ro et al., 2006[34]).


In summary, the main negative effects of mycoviruses are:

  • Decreased growth rate (Moleleki et al., 2003[36])
  • Lack of sporulation (Moleleki et al., 2003[36])
  • Attenuation of virulence (Suzaki et al., 2005[37])
  • Reduced germination of basidiospores (Ihrmark et al., 2004[38])


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[39]). In addition to negative effects, beneficial interactions do also occur. Well described examples are the killer phenotypes in yeasts (Schmitt et al., 2002[40]) and Ustilago (Marquina et al., 2002[41]). 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[40]). There are potentially interesting applications of killer isolates in medicine, food industry, and agriculture (Schmitt et al., 2002[40]; Dawe&Nuss, 2001[20]). And Marquez et al. (2007)[42] 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

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