Sear

Mycovirus

Mycoviruses (Ancient Greek: μύκης

mykes ("fungus") + Latin virus), also
known as mycophages, are viruses that
infect fungi. The majority of mycoviruses
have double-stranded RNA (dsRNA)
genomes and isometric particles, but
approximately 30% have positive-sense,
single-stranded RNA (+ssRNA)
genomes.[1][2]

True mycoviruses demonstrate an ability

to be transmitted 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 co-
diverge with their hosts, i.e. their
phylogeny is largely congruent with that
of their primary hosts.[3] However, many
virus families containing mycoviruses
have only sparsely been sampled.
Mycovirology[4] is the study of
mycoviruses. It is a special subdivision
of virology and seeks to understand and
describe the 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 in
cultivated mushrooms (Agaricus
bisporus) in the late 1940s and was
called the La France disease.[5] Hollings
found more than three different types of
viruses in the abnormal sporophores.
This report essentially marks the
beginning of mycovirology.[4]

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)[6]

Mushrooms have shown no resistance to

the virus, and so control has been limited
to hygienic practises to stop the spread
of the virus.

Perhaps the best known mycovirus is

Cryphonectria parasitica hypovirus 1
(CHV1). CHV1 is exceptional within
mycoviral research for its success as a
biocontrol agent against the fungus C.
parasitica, the causative agent of
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 relatively small
number of vegetative compatibility
groups (VCGs) on the continent. By
contrast, in North America the
distribution of the hypovirulent
phenotype is often prevented because an
incompatibility reaction prevents fungal
hyphae from fusing and exchanging their
cytoplasmic content. In the United
States, at least 35 VCGs were found.[7] A
similar situation seems to be present in
China and Japan, where 71 VCGs have
been identified so far.[8]

Taxonomy
The majority of mycoviruses have
double-stranded RNA (dsRNA) genomes
and isometric particles, but
approximately 30% have positive-sense,
single-stranded RNA (+ssRNA)
genomes.[1][2] So far there is only one
true example of a single-stranded DNA
(ssDNA) mycovirus. A geminivirus-
related virus was found in Sclerotinia
sclerotiorum conferring hypovirulence to
its host.[9] The updated 9th ICTV report
on virus taxonomy[10] lists over 90
mycovirus species covering 10 viral
families, of which 20% were not assigned
to a genus or sometimes not even to a
family.

Isometric forms predominate mycoviral

morphologies in comparison to rigid
rods, flexuous rods, club-shaped
particles, enveloped bacilliform particles,
and Herpesvirus-like viruses.[11] 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 has prevented their
classification so far.[1] So far, viruses of
the families Partitiviridae, Totiviridae, and
Narnaviridae 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 frequently infected with two or more
unrelated viruses and also with defective
dsRNA and/or satellite dsRNA.[12][13]
There are also viruses that simply use
fungi as vectors and are distinct from
mycoviruses because they cannot
reproduce in the fungal cytoplasm.[14]

It is generally assumed that the natural

host range of mycoviruses is confined to
closely related vegetability compatibility
groups or VCGs which allow for
cytoplasmic fusion,[15] but some
mycoviruses can replicate in
taxonomically different fungal hosts.[4]
Good examples are mitoviruses found in
the two fungal species Sclerotinia
homoeocarpa and Ophiostoma novo-
ulmi.[16] 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.[17] CHV1
can also propagate in the genera
Endothia and Valsa,[12] which belong to
the two distinct families
Cryphonectriaceae and Diaporthaceae,
respectively. Furthermore, some human
pathogenic fungi are also found to be
naturally infected with mycoviruses,
including AfuPmV-1 of Aspergillus
fumigatus[18] and TmPV1 of Talaromyces
marneffei[19] (formerly Penicillium
marneffei).

Origin and evolution

Viruses consisting of 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.[20] Although the origin of
viruses is still not well understood,[21]
recently presented data suggest that
viruses may have invaded the emerging
"supergroups" of eukaryotes from an
ancestral pool during a very early stage
of life on earth. According to Koonin,[21]
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.[1][11]
The "ancient co-evolution hypothesis"
could explain why mycoviruses are so
diverse.[11][22]
It has also been suggested that it is very
likely that plant viruses containing a
movement protein evolved from
mycoviruses by introducing an
extracellular phase into their life cycle
rather than eliminating it. Furthermore,
the recent discovery of an ssDNA
mycovirus has tempted some
researchers[9] to suggest that RNA and
DNA viruses might have common
evolutionary mechanisms. However,
there are many cases where mycoviruses
are grouped together with plant viruses.
For example, CHV1 showed phylogenetic
relatedness to the ssRNA genus
Potyvirus,[23] 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.[1]
Therefore, another theory arose that
these viruses moved from a plant host to
a 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.[12][24]
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[25]
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.[12] Transmission between
species of the same genus sharing the
same habitat has also been reported
including Cryphonectria (C. parasitica and
C. sp), Sclerotinia (Sclerotinia
sclerotiorum and S. minor), and
Ophistoma (O. ulmi and O. novo-
ulmi).[26][27] Intraspecies transmission
has also been reported[28] 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. Research[29]
using Aspergillus species 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[29] 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.[30] 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,[2][31] which could imply that they
‘got stuck’ and were not able to move
actively forward themselves. Others have
suggested that the transmission of viral
mitochondrial dsRNA may play an
important role in the movement of
mitoviruses found in Botrytis cinerea.[32]
Impact on host phenotype
Phenotypic effects of mycoviral
infections can vary from advantageous
to deleterious, but most of them are
asymptomatic 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.[33]
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. A neutral co-
existence might just be the result of a
long co-evolutionary process.[34][35]
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
asymptomatic 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.[12] Other
examples of deleterious effects of
mycoviruses are the ‘La France’ disease
of Agaricus biporus[5][36] and the
mushroom diseases caused by Oyster
mushroom spherical virus[37] and Oyster
mushroom isometric virus.[36]

In summary, the main negative effects of

mycoviruses are:

Decreased growth rate[38]

Lack of sporulation[38]
Change of virulence[39][40][19]
Reduced germination of
basidiospores[41]
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.[42] In addition
to negative effects, beneficial
interactions do also occur. Well
described examples are the killer
phenotypes in yeasts[43] and Ustilago.[44]
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.[43] There are potentially
interesting applications of killer isolates
in medicine, food industry, and
agriculture.[22][43] A three-part system
involving a mycovirus of an endophytic
fungus (Curvularia protuberata) of the
grass Dichanthelium lanuginosum has
been described, which provides a thermal
tolerance to the plant, enabling it to
inhabit adverse environmental niches.[45]
In medically important fungi, an
uncharacterized A78 virus of Aspergillus
fugmigatus causes mild hypervirulent
effect on pathogenicity when tested on
Galleria mellonella (Greater wax moth).[40]
Furthermore, TmPV1, a dsRNA
partitivirus, of Talaromyces marneffei
(formerly Penicillium marneffei) was
found to cause hyperviruelnece
phenotype on Talaromyces marneffei
when tested on a mouse model.[19]
These could imply mycoviruses may play
important roles in the pathogensis of
human pathogenic fungi.

References
1. Pearson MN, Beever RE, Boine B,
 Arthur K (January 2009).
"Mycoviruses of filamentous fungi
and their relevance to plant
pathology" . Molecular Plant
Pathology. 10 (1): 115–28.
doi:10.1111/j.1364-
3703.2008.00503.x . PMC 6640375 .
PMID 19161358 .
2. Bozarth RF (October 1972).
"Mycoviruses: a new dimension in
microbiology" . Environmental Health
Perspectives. 2 (1): 23–39.
doi:10.1289/ehp.720223 .
PMC 1474899 . PMID 4628853 .
3. Göker M, Scheuner C, Klenk HP,
Stielow JB, Menzel W (2011).
"Codivergence of mycoviruses with
their hosts" . PLOS ONE. 6 (7):
e22252.
Bibcode:2011PLoSO...622252G .
doi:10.1371/journal.pone.0022252 .
PMC 3146478 . PMID 21829452 .
4. Ghabrial SA, Suzuki N (2009).
"Viruses of plant pathogenic fungi".
Annual Review of Phytopathology.
47: 353–84. doi:10.1146/annurev-
phyto-080508-081932 .
PMID 19400634 .
5. Hollings M (1962). "Viruses
Associated with A Die-Back Disease
of Cultivated Mushroom". Nature.
196 (4858): 962–965.
Bibcode:1962Natur.196..962H .
doi:10.1038/196962a0 .
6. Romaine CP, Schlagnhaufer B (June
1995). "PCR analysis of the viral
complex associated with La France
disease of Agaricus bisporus" .
Applied and Environmental
Microbiology. 61 (6): 2322–5.
PMC 167503 . PMID 7793952 .
7. Anagnostakis SL, Chen B, Geletka
LM, Nuss DL (July 1998). "Hypovirus
Transmission to Ascospore Progeny
by Field-Released Transgenic
Hypovirulent Strains of Cryphonectria
parasitica". Phytopathology. 88 (7):
598–604.
doi:10.1094/PHYTO.1998.88.7.598 .
PMID 18944931 .
8. Liu YC, Milgroom MG (2007). "High
diversity of vegetative compatibility
types in Cryphonectria parasitica in
Japan and China". Mycologia. 99 (2):
279–84.
 doi:10.3852/mycologia.99.2.279 .
PMID 17682780 .
9. Yu X, Li B, Fu Y, Jiang D, Ghabrial SA,
Li G, Peng Y, Xie J, Cheng J, Huang J,
Yi X (May 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):
8387–92.
Bibcode:2010PNAS..107.8387Y .
doi:10.1073/pnas.0913535107 .
PMC 2889581 . PMID 20404139 .
10. [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.
11. Varga J, Tóth B, Vágvölgyi C (2003).
"Recent advances in mycovirus
research". Acta Microbiologica et
Immunologica Hungarica. 50 (1):
77–94.
doi:10.1556/AMicr.50.2003.1.8 .
PMID 12793203 .
12. 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.
13. Howitt RL, Beever RE, Pearson MN,
Forster RL (March 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–
 79. doi:10.1007/s00705-005-0621-y .
PMID 16172841 .
14. Adams, M. J. (1991). "Transmission
of plant viruses by fungi". Annals of
Applied Biology. 118 (2): 479–492.
doi:10.1111/j.1744-
7348.1991.tb05649.x .
15. Buck, K. W. (1986). Fungal Virology-
An overview', in K. Buck (ed.), Fungal
Virology (Boca Raton: CRC Press): 1-
84.
16. Deng F, Xu R, Boland GJ (November
2003). "Hypovirulence-Associated
 Double-Stranded RNA from
Sclerotinia homoeocarpa Is
Conspecific with Ophiostoma novo-
ulmi Mitovirus 3a-Ld".
Phytopathology. 93 (11): 1407–14.
doi:10.1094/PHYTO.2003.93.11.140
7 . PMID 18944069 .
17. Chen B, Choi GH, Nuss DL (June
1994). "Attenuation of fungal
virulence by synthetic infectious
hypovirus transcripts". Science. 264
(5166): 1762–4.
Bibcode:1994Sci...264.1762C .
 doi:10.1126/science.8209256 .
PMID 8209256 .
18. Kotta-Loizou I, Coutts RH (2017).
"Aspergilli: A Comprehensive
Review" . Frontiers in Microbiology.
8: 1699.
doi:10.3389/fmicb.2017.01699 .
PMC 5592211 . PMID 28932216 .
19. Lau SK, Lo GC, Chow FW, Fan RY, Cai
JJ, Yuen KY, Woo PC (June 2018).
"Novel Partitivirus Enhances
Virulence of and Causes Aberrant
Gene Expression in Talaromyces
marneffei" . mBio. 9 (3): e00947–18.
 doi:10.1128/mBio.00947-18 .
PMC 6016240 . PMID 29895639 .
20. Forterre P (April 2006). "The origin of
viruses and their possible roles in
major evolutionary transitions". Virus
Research. 117 (1): 5–16.
doi:10.1016/j.virusres.2006.01.010 .
PMID 16476498 .
21. Koonin EV, Wolf YI (December 2008).
"Genomics of bacteria and archaea:
the emerging dynamic view of the
prokaryotic world" . Nucleic Acids
Research. 36 (21): 6688–719.
 doi:10.1093/nar/gkn668 .
PMC 2588523 . PMID 18948295 .
22. Dawe AL, Nuss DL (2001).
"Hypoviruses and chestnut blight:
exploiting viruses to understand and
modulate fungal pathogenesis".
Annual Review of Genetics. 35: 1–29.
doi:10.1146/annurev.genet.35.10240
1.085929 . PMID 11700275 .
23. Fauquet CM, Mayo MA, 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.
24. Ghabrial SA (1994). "New
Developments in Fungal Virology". In
Murphy FA, Maramorosch K, Aaron
JS (eds.). Advances in Virus
Research. 43. Academic Press.
pp. 303–388.
25. Liu H, Fu Y, Jiang D, Li G, Xie J, Peng
Y, Yi X, Ghabrial SA (February 2009).
"A novel mycovirus that is related to
the human pathogen hepatitis E virus
and rubi-like viruses" . Journal of
Virology. 83 (4): 1981–91.
 doi:10.1128/JVI.01897-08 .
PMC 2643757 . PMID 19073734 .
26. Liu YC, Linder-Basso D, Hillman BI,
Kaneko S, Milgroom MG (June 2003).
"Evidence for interspecies
transmission of viruses in natural
populations of filamentous fungi in
the genus Cryphonectria". Molecular
Ecology. 12 (6): 1619–28.
doi:10.1046/j.1365-
294x.2003.01847.x .
PMID 12755889 .
27. Melzer MS, Deng F, Boland GJ
(December 2005). "Asymptomatic
 infection, and distribution of
Ophiostoma mitovirus 3a (OMV3a),
in populations of Sclerotinia
homoeocarpa". Canadian Journal of
Plant Pathology. 27 (4): 610–5.
doi:10.1080/07060660509507262 .
28. Van Diepeningen AD, Debets AJ,
Slakhorst SM, Fekete C, Hornok L,
Hoekstra RF (2000). "Interspecies
virus transfer via protoplast fusions
between Fusarium poae and black
Aspergillus strains". Fungal Genetics
Newsletter. 47: 99–100.
29. van Diepeningen AD, Debets AJ,
Hoekstra RF (June 2006). "Dynamics
of dsRNA mycoviruses in black
Aspergillus populations". Fungal
Genetics and Biology. 43 (6): 446–
52. doi:10.1016/j.fgb.2006.01.014 .
PMID 16546419 .
30. Sasaki A, Kanematsu S, Onoue M,
Oyama Y, Yoshida K (April 2006).
"Infection of Rosellinia necatrix with
purified viral particles of a member
of Partitiviridae (RnPV1-W8)".
Archives of Virology. 151 (4): 697–
 707. doi:10.1007/s00705-005-0662-
2 . PMID 16307176 .
31. Vilches S, Castillo A (October 1997).
"A double-stranded RNA mycovirus in
Botrytis cinerea". FEMS Microbiology
Letters. 155 (1): 125–30.
doi:10.1016/S0378-1097(97)00377-
7 . PMID 9345772 .
32. Wu M, Zhang L, Li G, Jiang D,
Ghabrial SA (October 2010).
"Genome characterization of a
debilitation-associated mitovirus
infecting the phytopathogenic fungus
Botrytis cinerea". Virology. 406 (1):
 117–26.
doi:10.1016/j.virol.2010.07.010 .
PMID 20674953 .
33. McCabe PM, Pfeiffer P, Van Alfen NK
(September 1999). "The influence of
dsRNA viruses on the biology of
plant pathogenic fungi". Trends in
Microbiology. 7 (9): 377–81.
doi:10.1016/S0966-842X(99)01568-
1 . PMID 10470047 .
34. May RM, Nowak MA (August 1995).
"Coinfection and the evolution of
parasite virulence" (PDF).
Proceedings. Biological Sciences.
 261 (1361): 209–15.
doi:10.1098/rspb.1995.0138 .
PMID 7568274 .
35. Araújo, A., Jansen, A. M., Bouchet, F.,
Reinhard, K., Ferreira, L. F. (2003).
Parasitism, the Diversity of Life, and
Paleoparasitology. Memórias do
Instituto Oswaldo Cruz, 98 (SUPPL.
1): 5-11.
36. Ro HS, Lee NJ, Lee CW, Lee HS
(December 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): 24–9.
doi:10.1016/j.jviromet.2006.07.016 .
PMID 16930731 .
37. Yu HJ, Lim D, Lee HS (September
2003). "Characterization of a novel
single-stranded RNA mycovirus in
Pleurotus ostreatus". Virology. 314
(1): 9–15. doi:10.1016/S0042-
6822(03)00382-9 . PMID 14517055 .
38. Moleleki N, van Heerden SW,
Wingfield MJ, Wingfield BD, Preisig O
(July 2003). "Transfection of
Diaporthe perjuncta with Diaporthe
 RNA virus" . Applied and
Environmental Microbiology. 69 (7):
3952–6.
doi:10.1128/AEM.69.7.3952-
3956.2003 . PMC 165159 .
PMID 12839766 .
39. Suzaki K, Ikeda KI, Sasaki A,
Kanematsu S, Matsumoto N, Yoshida
K (June 2005). "Horizontal
transmission and host-virulence
attenuation of totivirus in violet root
rot fungus Helicobasidium mompa".
Journal of General Plant Pathology.
 71 (3): 161–168.
doi:10.1007/s10327-005-0181-8 .
40. Özkan S, Coutts RH (March 2015).
"Aspergillus fumigatus mycovirus
causes mild hypervirulent effect on
pathogenicity when tested on
Galleria mellonella". Fungal Genetics
and Biology. 76: 20–6.
doi:10.1016/j.fgb.2015.01.003 .
hdl:2299/16060 . PMID 25626171 .
41. Ihrmark K, Stenström E, Stenlid J
(February 2004). "Double-stranded
RNA transmission through
basidiospores of Heterobasidion
 annosum". Mycological Research.
108 (Pt 2): 149–53.
doi:10.1017/S0953756203008839 .
PMID 15119351 .
42. Xie J, Wei D, Jiang D, Fu Y, Li G,
Ghabrial S, Peng Y (January 2006).
"Characterization of debilitation-
associated mycovirus infecting the
plant-pathogenic fungus Sclerotinia
sclerotiorum". The Journal of General
Virology. 87 (Pt 1): 241–9.
doi:10.1099/vir.0.81522-0 .
PMID 16361437 .
43. Schmitt MJ, Breinig F (August 2002).
"The viral killer system in yeast: from
molecular biology to application".
FEMS Microbiology Reviews. 26 (3):
257–76. doi:10.1016/S0168-
6445(02)00099-2 . PMID 12165427 .
44. Marquina D, Santos A, Peinado JM
(June 2002). "Biology of killer
yeasts" (PDF). International
Microbiology. 5 (2): 65–71.
doi:10.1007/s10123-002-0066-z .
PMID 12180782 .
45. Márquez LM, Redman RS, Rodriguez
RJ, Roossinck MJ (January 2007). "A
 virus in a fungus in a plant: three-way
symbiosis required for thermal
tolerance" . Science. 315 (5811):
513–5.
Bibcode:2007Sci...315..513M .
doi:10.1126/science.1136237 .
PMID 17255511 .

Further reading
Boine, Barbara (2012). A study of the
interaction between the plant pathogenic
fungus Botrytis cinerea and the filamentous
ssRNA mycoviruses Botrytis virus X and
Botrytis virus F (PhD thesis). The
 University of Auckland, School of Biological
Sciences, Plant and Fungal Virology.

External links
"International Committee on Taxonomy
of Viruses" .

Retrieved from
"https://en.wikipedia.org/w/index.php?
title=Mycovirus&oldid=930694811"

Last edited 25 days ago by Citation bot

Content is available under CC BY-SA 3.0 unless

otherwise noted.