The European race of the ascomycetous species Gremmeniella abietina (Lagerberg) Morelet includes causal agents of shoot blight and stem canker of several conifers in Europe and North America, which are known to host a diverse virome. GaRV6 is the latest and sixth mycovirus species reported within G. abietina. Before its description, one victorivirus and one gammapartitivirus species were described in biotype A, two mitoviruses in both biotypes A and B and a betaendornavirus in biotype B. Possible phenotypic changes produced by mycoviruses on G. abietina mycelial growth have been reported in Spanish mitovirus-free and GaRV6-hosting G. abietina isolates, which had higher growth rates at the optimal temperature of 15 °C, but no other major differences have been observed between partitivirus-like dsRNA and dsRNA-free isolates. In this review, we reappraise the diversity of viruses found in G. abietina so far, and their relevance in clarifying the taxonomy of G. abietina. We also provide evidence for the presence of two new viruses belonging to the families Fusariviridae and Endornaviridae in Spanish isolates.

Forest Health and Biodiversity Natural Resources Institute Finland Latokartanonkaari 9 00790 Helsinki Finland

Phytophthora Research Centre Department of Forest Protection and Wildlife Management Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 1 613 00 Brno Czech Republic

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Donaubauer E. Distribution and hosts of Scleroderris lagerbergii in Europe and North America. For. Pathol. 1972;2:6–11. doi: 10.1111/j.1439-0329.1972.tb00336.x. DOI

Yokota S., Uozumi T., Matsuzaki S. Scleroderris canker of Todo-Fir in Hokkaido, Northern Japan I. Present status of damage, and features of infected plantations. For. Pathol. 1974;4:65–74. doi: 10.1111/j.1439-0329.1974.tb00421.x. DOI

Morelet M. La maladie à Brunchorstia. Eur. J. For. Pathol. 1980;10:268–277. doi: 10.1111/j.1439-0329.1980.tb00039.x. DOI

Barklund P., Rowe J. Gremmeniella abietina (Scleroderris lagerbergii), a primary parasite in a Norway spruce die-back. For. Pathol. 1981;11:97–108. doi: 10.1111/j.1439-0329.1981.tb00075.x. DOI

Kaitera J., Seitamäki L., Jalkanen R. Morphological and ecological variation of Gremmeniella abietina var. abietina in Pinus sylvestris, Pinus contorta and Picea abies sapling stands in northern Finland and the Kola Peninsula. Scand. J. For. Res. 2000;15:13–19. doi: 10.1080/02827580050160420. DOI

Santamaria O., Alves-Santos F.M., Diez J.J. Genetic characterization of Gremmeniella abietina var. abietina isolates from Spain. Plant Pathol. 2005;54:331–338. doi: 10.1111/j.1365-3059.2005.01184.x. DOI

Petrini O., Toti L., Petrini L.E., Heiniger U. Gremmeniella abietina and G. laricina in Europe: characterization and identification of isolates and laboratory strains by soluble protein electrophoresis. Can. J. Bot. 1990;68:2629–2635. doi: 10.1139/b90-332. DOI

Dorworth C.E., Krywienczyk J. Comparisons among isolates of Gremmeniella abietina by means of growth rate, conidia measurement, and immunogenic reaction. Can. J. Bot. 1975;53:2506–2525. doi: 10.1139/b75-276. DOI

Uotila A., Hantula J., Vaatanen A.K., Hamelin R.C. Hybridization between two biotypes of Gremmeniella abietina var. abietina in artificial pairings. For. Pathol. 2000;30:211–219. doi: 10.1046/j.1439-0329.2000.00207.x. DOI

Hamelin R.C., Rail J. Phylogeny of Gremmeniella spp. based on sequences of the 5.8S rDNA and internal transcribed spacer region. Can. J. Bot. 1997;75:693–698. doi: 10.1139/b97-078. DOI

Uotila A. Physiological and morphological variation among Finnish Gremmeniella abietina isolates. Commun. Inst. For. Fenn. 1983;119:12.

Hamelin R.C., Lecours N., Hansson P., Hellgren M., Laflamme G. Genetic differentiation within the European race of Gremmeniella abietina. Mycol. Res. 1996;100:49–56. doi: 10.1016/S0953-7562(96)80099-2. DOI

Hellgren M., Högberg N. Ecotypic variation of Gremmeniella abietina in northern Europe: Disease patterns reflected by DNA variation. Can. J. Bot. 1995;73:1531–1539. doi: 10.1139/b95-166. DOI

Hantula J., Muller M. Variation within Gremmeniella abietina in Finland and other countries as determined by Random Amplified Microsatellites (RAMS) Mycol. Res. 1997;101:169–175. doi: 10.1017/S0953756296002225. DOI

Santamaria O., Pajares J.A., Diez J.J. First report of Gremmeniella abietina on Pinus halepensis in Spain. Plant Pathol. 2003;52:425. doi: 10.1046/j.1365-3059.2003.00847.x. DOI

Botella L., Tuomivirta T.T., Kaitera J., Carrasco Navarro V., Diez J.J., Hantula J. Spanish population of Gremmeniella abietina is genetically unique but related to type A in Europe. Fungal Biol. 2010;114:778–789. doi: 10.1016/j.funbio.2010.07.003. PubMed DOI

Ghabrial S.A., Suzuki N. Viruses of Plant Pathogenic Fungi. Annu. Rev. Phytopathol. 2009;47:353–384. doi: 10.1146/annurev-phyto-080508-081932. PubMed DOI

Schoebel C.N., Botella L., Lygis V., Rigling D. Population genetic analysis of a parasitic mycovirus to infer the invasion history of its fungal host. Mol. Ecol. 2017;26:2482–2497. doi: 10.1111/mec.14048. PubMed DOI

Bryner S.F., Rigling D., Brunner P.C. Invasion history and demographic pattern of Cryphonectria hypovirus 1 across European populations of the chestnut blight fungus. Ecol. Evol. 2012;2:3227–3241. doi: 10.1002/ece3.429. PubMed DOI PMC

Vainio E.J., Hyder R., Aday G., Hansen E., Piri T., Doğmuş-Lehtijärvi T., Lehtijärvi A., Korhonen K., Hantula J. Population structure of a novel putative mycovirus infecting the conifer root-rot fungus Heterobasidion annosum sensu lato. Virology. 2012;422:366–376. doi: 10.1016/j.virol.2011.10.032. PubMed DOI

Milgroom M.G., Lipari S.E., Ennos R.A., Liu Y.-C. Estimation of the outcrossing rate in the chestnut blight fungus, Cryphonectria parasitica. Heredity. 1993;70:385–892. doi: 10.1038/hdy.1993.54. DOI

Liu Y.-C., Linder-Basso D., Hillman B.I., Kaneko S., Milgroom M.G. Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria. Mol. Ecol. 2003;12:1619–1628. doi: 10.1046/j.1365-294X.2003.01847.x. PubMed DOI

Deng F., Xu R., Boland G.J. Hypovirulence-associated double-stranded RNA from Sclerotinia homoeocarpa is conspecific with Ophiostoma novo-ulmi Mitovirus 3a-Ld. Phytopathology. 2003;93:1407–1414. doi: 10.1094/PHYTO.2003.93.11.1407. PubMed DOI

Buck K.W., Brasier C.M., Paoletti M., Crawford L.J. Virus transmission and gene flow between two species of the Dutch elm disease fungi, Ophiostoma ulmi and O. novo-ulmi: Deleterious viruses as selective. Br. Ecol. Soc. 2003;15:26–45.

Vainio E.J., Hakanpää J., Dai Y.-C., Hansen E., Korhonen K., Hantula J. Species of Heterobasidion host a diverse pool of partitiviruses with global distribution and interspecies transmission. Fungal Biol. 2011;115:1234–1243. doi: 10.1016/j.funbio.2011.08.008. PubMed DOI

Kashif M., Hyder R., De Vega Perez D., Hantula J., Vainio E.J. Heterobasidion wood decay fungi host diverse and globally distributed viruses related to Helicobasidium mompa partitivirus V70. Virus Res. 2015;195:119–123. doi: 10.1016/j.virusres.2014.09.002. PubMed DOI

Melzer M.S., Ikeda S.S., Boland G.J. Interspecific transmission of double-stranded RNA and hypovirulence from Sclerotinia sclerotiorum to S. minor. Phytopathology. 2002;92:780–784. doi: 10.1094/PHYTO.2002.92.7.780. PubMed DOI

Boland G.J. Fungal viruses, hypovirulence, and biological control of Sclerotinia species. Can. J. Plant Pathol. 2004;26:6–18. doi: 10.1080/07060660409507107. DOI

Charlton N.D., Carbone I., Tavantzis S.M., Cubeta M.A. Phylogenetic relatedness of the M2 double-stranded RNA in Rhizoctonia fungi. Mycologia. 2008;100:555–564. doi: 10.3852/07-108R. PubMed DOI

Tuomivirta T.T., Uotila A., Hantula J. Two independent double-stranded RNA patterns occur in the Finnish Gremmeniella abietina var. abietina type A. For. Pathol. 2002;32:197–205. doi: 10.1046/j.1439-0329.2002.00285.x. DOI

Tuomivirta T.T., Hantula J. Two unrelated double-stranded RNA molecule patterns in Gremmeniella abietina type A code for putative viruses of the families Totiviridae and Partitiviridae. Arch. Virol. 2003;148:2293–2305. doi: 10.1007/s00705-003-0194-6. PubMed DOI

Tuomivirta T.T., Hantula J. Three unrelated viruses occur in a single isolate of Gremmeniella abietina var. abietina type A. Virus Res. 2005;110:31–39. doi: 10.1016/j.virusres.2004.12.005. PubMed DOI

Tuomivirta T.T., Hantula J. Gremmeniella abietina mitochondrial RNA virus S1 is phylogenetically related to the members of the genus Mitovirus. Arch. Virol. 2003;148:2429–2436. doi: 10.1007/s00705-003-0195-5. PubMed DOI

Botella L., Tuomivirta T.T., Vervuurt S., Diez J.J., Hantula J. Occurrence of two different species of mitoviruses in the European race of Gremmeniella abietina var. abietina, both hosted by the genetically unique Spanish population. Fungal Biol. 2012;116:872–882. doi: 10.1016/j.funbio.2012.05.004. PubMed DOI

Tuomivirta T.T., Kaitera J., Hantula J. A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities. J. Gen. Virol. 2009;90:2299–2305. doi: 10.1099/vir.0.011973-0. PubMed DOI

Botella L., Vainio E.J., Hantula J., Diez J.J., Jankovsky L. Description and prevalence of a putative novel mycovirus within the conifer pathogen Gremmeniella abietina. Arch. Virol. 2015;160:1967–1975. doi: 10.1007/s00705-015-2456-5. PubMed DOI

Nibert M.L., Ghabrial S.A., Maiss E., Lesker T., Vainio E.J., Jiang D., Suzuki N. Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res. 2014;188:128–141. doi: 10.1016/j.virusres.2014.04.007. PubMed DOI

Botella L., Tuomivirta T.T., Hantula J., Diez J.J., Jankovsky L. The European race of Gremmeniella abietina hosts a single species of gammapartitivirus showing a global distribution and possible recombinant events in its history. Fungal Biol. 2015;119:125–135. doi: 10.1016/j.funbio.2014.12.001. PubMed DOI PMC

Kuraku S., Zmasek C.M., Nishimura O., Katoh K. aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res. 2013;41:W22–W28. doi: 10.1093/nar/gkt389. PubMed DOI PMC

Thapa V., Turner G.G., Hafenstein S., Overton B.E., Vanderwolf K.J., Roossinck M.J. Using a novel partitivirus in Pseudogymnoascus destructans to understand the epidemiology of White-Nose Syndrome. PLoS Pathog. 2016;12:e1006076. doi: 10.1371/journal.ppat.1006076. PubMed DOI PMC

Marzano S.-Y.L., Domier L.L. Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res. 2016;213:332–342. doi: 10.1016/j.virusres.2015.11.002. PubMed DOI

Komatsu K., Katayama Y., Omatsu T., Mizutani T., Fukuhara T., Kodama M., Arie T., Teraoka T., Moriyama H. Genome sequence of a novel mitovirus identified in the phytopathogenic fungus Alternaria arborescens. Arch. Virol. 2016;161:2627–2631. doi: 10.1007/s00705-016-2953-1. PubMed DOI

Chen Y., Shang H.H., Yang H.Q., Da Gao B., Zhong J. A mitovirus isolated from the phytopathogenic fungus Alternaria brassicicola. Arch. Virol. 2017;162:2869–2874. doi: 10.1007/s00705-017-3371-8. PubMed DOI

Bruenn J.A. A closely related group of RNA-dependent RNA polymerases from double-stranded RNA viruses. Nucleic Acids Res. 1993;21:5667–5669. doi: 10.1093/nar/21.24.5667. PubMed DOI PMC

Nerva L., Ciuffo M., Vallino M., Margaria P., Varese G.C., Gnavi G., Turina M. Multiple approaches for the detection and characterization of viral and plasmid symbionts from a collection of marine fungi. Virus Res. 2016;219:22–38. doi: 10.1016/j.virusres.2015.10.028. PubMed DOI

Niu Y., Zhang T., Zhu Y., Yuan Y., Wang S., Liu J., Liu D. Isolation and characterization of a novel mycovirus from Penicillium digitatum. Virology. 2016;494:15–22. doi: 10.1016/j.virol.2016.04.004. PubMed DOI

Hammond T.M., Andrewski M.D., Roossinck M.J., Keller N.P. Aspergillus mycoviruses are targets and suppressors of RNA silencing. Eukaryot. Cell. 2008;7:350–357. doi: 10.1128/EC.00356-07. PubMed DOI PMC

Rong R., Rao S., Scott S.W., Carner G.R., Tainter F.H. Complete sequence of the genome of two dsRNA viruses from Discula destructiva. Virus Res. 2002;90:217–224. doi: 10.1016/S0168-1702(02)00178-8. PubMed DOI

Khalifa M.E., Pearson M.N. Molecular characterisation of an endornavirus infecting the phytopathogen Sclerotinia sclerotiorum. Virus Res. 2014;189:303–309. doi: 10.1016/j.virusres.2014.06.010. PubMed DOI

Yu J., Kwon S.-J., Lee K.-M., Son M., Kim K.-H. Complete nucleotide sequence of double-stranded RNA viruses from Fusarium graminearum strain DK3. Arch. Virol. 2009;154:1855–1858. doi: 10.1007/s00705-009-0507-5. PubMed DOI

Zheng L., Liu H., Zhang M., Cao X., Zhou E. The complete genomic sequence of a novel mycovirus from Rhizoctonia solani AG-1 IA strain B275. Arch. Virol. 2013;158:1609–1612. doi: 10.1007/s00705-013-1637-3. PubMed DOI

Marquez L.M., Redman R.S., Rodriguez R., Stout R.G., Rodriguez R.J., Roossinck M. A Virus in a fungus in a plant: Three-way symbiosis required for thermal tolerance. Science. 2007;315:513–515. doi: 10.1126/science.1136237. PubMed DOI

Wang L., Wang S., Yang X., Zeng H., Qiu D., Guo L. The complete genome sequence of a double-stranded RNA mycovirus from Fusarium graminearum strain HN1. Arch. Virol. 2017;162:2119–2124. doi: 10.1007/s00705-017-3317-1. PubMed DOI

Jiang Y., Zhang T., Luo C., Jiang D., Li G., Li Q., Hsiang T., Huang J. Prevalence and diversity of mycoviruses infecting the plant pathogen Ustilaginoidea virens. Virus Res. 2015;195:47–56. doi: 10.1016/j.virusres.2014.08.022. PubMed DOI

Botella L., Dvořák M., Capretti P., Luchi N. Effect of temperature on GaRV6 accumulation and its fungal host, the conifer pathogen Gremmeniella abietina. For. Pathol. 2017;47:e12291. doi: 10.1111/efp.12291. DOI

Leticia Botella L., Tuomivirta T.T., Hantula J., Diez J.J. Presence of viral dsRNA molecules in the Spanish population of Gremmeniella abietina. J. Agric. Ext. Rural Dev. 2012;4:211–213. doi: 10.5897/JAERD12.051. DOI

Göker M., Scheuner C., Klenk H.-P., Stielow J.B., Menzel W. Codivergence of mycoviruses with their hosts. PLoS ONE. 2011;6:e22252. doi: 10.1371/journal.pone.0022252. PubMed DOI PMC

Pearson M.N., Beever R.E., Boine B., Arthur K. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol. Plant Pathol. 2009;10:115–128. doi: 10.1111/j.1364-3703.2008.00503.x. PubMed DOI PMC

Varga J., Vágvölgyi C., Tóth B. Recent advances in mycovirus research. Acta Microbiol. Immunol. Hung. 2003;50:77–94. doi: 10.1556/AMicr.50.2003.1.8. PubMed DOI

Linder-Basso D., Dynek J.N., Hillman B.I. Genome analysis of Cryphonectria hypovirus 4, the most common hypovirus species in North America. Virology. 2005;337:192–203. doi: 10.1016/j.virol.2005.03.038. PubMed DOI

Dorworth C.E., Krywienczyk J., Skilling D.D. New York isolates of Gremmeniella abietina (Scleroderris lagerbergii) identical in immunogenic reaction to European isolates [Pinus] Plant Dis. Rep. 1977;61:887–890.

Marosy M., Patton R.F., Upper C.D. A conductive day concept to explain the effect of low temperature on the development of Scleroderris shoot blight. Ecol. Epidemiol. 1989;79:1293–1301.

Yaegashi H., Kanematsu S. Natural infection of the soil-borne fungus Rosellinia necatrix with novel mycoviruses under greenhouse conditions. Virus Res. 2016;219:83–91. doi: 10.1016/j.virusres.2015.11.004. PubMed DOI

Yaegashi H., Nakamura H., Sawahata T., Sasaki A., Iwanami Y., Ito T., Kanematsu S. Appearance of mycovirus-like double-stranded RNAs in the white root rot fungus, Rosellinia necatrix, in an apple orchard. FEMS Microbiol. Ecol. 2013;83:49–62. doi: 10.1111/j.1574-6941.2012.01454.x. PubMed DOI

Vainio E.J., Pennanen T., Rajala T., Hantula J. Occurrence of similar mycoviruses in pathogenic, saprotrophic and mycorrhizal fungi inhabiting the same forest stand. FEMS Microbiol. Ecol. 2017;93:fix003. doi: 10.1093/femsec/fix003. PubMed DOI

Romeralo Tapia C., Botella L., Santamaría O., Diez J. Effect of putative mitoviruses on in vitro growth of Gremmeniella abietina isolates under different laboratory conditions. For. Syst. 2012;21:515. doi: 10.5424/fs/2012213-02266. DOI

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