The population genetics of the family Partitiviridae was studied within the European race of the conifer pathogen Gremmeniella abietina. One hundred sixty-two isolates were collected from different countries, including Canada, the Czech Republic, Finland, Italy, Montenegro, Serbia, Spain, Switzerland, Turkey and the United States. A unique species of G. abietina RNA virus-MS1 (GaRV-MS1) appears to occur indistinctly in G. abietina biotypes A and B, without a particular geographical distribution pattern. Forty-six isolates were shown to host GaRV-MS1 according to direct specific RT-PCR screening, and the virus was more common in biotype A than B. Phylogenetic analysis based on 46 partial coat protein (CP) cDNA sequences divided the GaRV-MS1 population into two closely related clades, while RNA-dependent RNA polymerase (RdRp) sequences revealed only one clade. The evolution of the virus appears to mainly occur through purifying selection but also through recombination. Recombination events were detected within alignments of the three complete CP and RdRp sequences of GaRV-MS1. This is the first time that recombination events have been directly identified in fungal partitiviruses and in G. abietina in particular. The results suggest that the population dynamics of GaRV-MS1 do not have a direct impact on the genetic structure of its host, G. abietina, though they might have had an innocuous ancestral relationship.

Department of Forest Protection and Wildlife Management Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 1 61300 Brno Czech Republic

Finnish Forest Research Institute Vantaa Research Unit PO Box 18 01301 Vantaa Finland

Sustainable Forest Management Research Institute University of Valladolid INIA Avenida de Madrid 44 34071 Palencia Spain

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Alabi O.J., Martin R.R., Naidu R.A. Sequence diversity, population genetics and potential recombination events in grapevine rupestris stem pitting-associated virus in Pacific North-West vineyards. The Journal of General Virology. 2010;91:265–276. PubMed

Banner L.R., Lai M.M.C. Random nature of coronavirus RNA recombination in the absence of selection pressure. Virology. 1991;185:441–445. PubMed PMC

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 Biology. 2010;114:778–789. PubMed

Botella L., Tuomivirta T.T., Hantula J., Diez J.J. Presence of viral dsRNA molecules in the Spanish population of Gremmeniella abietina. Journal of Agricultural Extension and Rural Development. 2012;4:211–213.

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 Biology. 2012;116:872–882. PubMed

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. Ecology and Evolution. 2012;2:3227–3241. PubMed PMC

Buck K.W. Molecular variability of viruses of fungi. In: Bridge P.D., Couteaudier Y., Clackson J.M., editors. Molecular Variability of Fungal Pathogens. CAB International; Wallingford, UK: 1998.

Carbone I., Liu Y.-C., Hillman B.I., Milgroom M.G. Recombination and migration of Cryphonectria hypovirus 1 as inferred from gene genealogies and the coalescent. Genetics. 2004;166:1611–1629. PubMed PMC

Chare E.R. Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. Journal of General Virology. 2003;84:2691–2703. PubMed

Chiba S., Lin Y.-H., Kondo H., Kanematsu S., Suzuki N. Effects of defective interfering RNA on symptom induction by, and replication of, a novel partitivirus from a phytopathogenic fungus, Rosellinia necatrix. Journal of virology. 2013;87:2330–2341. PubMed PMC

Cortesi P., Milgroom M.G. Genetics of vegetative incompatibility in Cryphonectria parasitica. Applied and Environmental Microbiology. 1998;64:2988–2994. PubMed PMC

Dogmus-Lehtijarvi H.T., Oskaz F., Karadeniz M., Lehtijarvi A. Susceptibility of Pinus nigra and Cedrus libani to Turkish Gremmeniella abietina isolates. Forest Systems. 2012;21:306–312.

Donaubauer E. Distribution and hosts of Scleroderris lagerbergii in Europe and North America. European Journal of Forest Pathology. 1972;9:316–322.

Feau N., Dutech C., Brusini J., Rigling D., Robin C. Multiple introductions and recombination in Cryphonectria hypovirus 1: perspective for a sustainable biological control of chestnut blight. Evolutionary Applications. 2014;7:580–596. PubMed PMC

Ghabrial S.A. Origin, adaptation and evolutionary pathways of fungal viruses. Virus Genes. 1998;16:119–131. PubMed PMC

Göker M., Scheuner C., Klenk H., Stielow J.B., Menzel W. Codivergence of mycoviruses with their hosts. PLOS One. 2011;6:e22252. PubMed PMC

Gruber A.R., Lorenz R., Bernhart S.H., Neuböck R., Hofacker I.L. The Vienna RNA Websuite. Nucleic Acids Research. 2008;36 Web Server Issue. PubMed PMC

Hamelin R.C., Lecours N., Hansson P., Hellgren M., Laflamme G. Genetic differentiation within the European race of Gremmeniella abietina. Mycological Research. 1996;100:49–56.

Hantula J., Tuomivirta T.T. The species complex of Gremmeniella abietina -intertype hybridization, viruses, and gene flow in northern Europe. Canadian Journal of Botany. 2003;81:1213–1215.

Hellgren M., Högberg N. Ecotypic variation of Gremmeniella abietina in northern Europe: disease patterns reflected by DNA variation. Canadian Journal of Botany. 1995;73:1531–1539.

Ihrmark K., Johannesson H., Stenström E., Stenlid J. Transmission of double-stranded RNA in Heterobasidion annosum. Fungal Genetics and Biology. 2002;36:147–154. PubMed

Jukes T.H., Cantor C.R. Evolution of protein molecules. In: Munro H.N., editor. Mammalian Protein Metabolism. Academic Press; New York: 1969. pp. 21–132.

Kaitera J., Jalkanen R. In vitro growth of Gremmeniella abietina isolates (European race) at different temperatures. Scandinavian Journal of Forest Research. 1996;11:159–163.

Kimura M. Cambridge University Press; UK: 1983. The Neutral Theory of Molecular Evolution.

Leslie J.F., Zeller K.A. Heterokaryon incompatibility in fungi: More than just another way to die. Journal of Genetics. 1996;75:415–424.

Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–1452. PubMed

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. PubMed

Liu H., Fu Y., Xie J., Cheng J., Ghabrial S.A., Li G., Peng Y., Yi X., Jiang D. Evolutionary genomics of mycovirus-related dsRNA viruses reveals cross-family horizontal gene transfer and evolution of diverse viral lineages. BMC Evolutionary Biology. 2012;12:91. PubMed PMC

Martin D., Lemey P., Lott M., Moulton V., Posada D., Lefeuvre P. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics. 2010;26:2462–2463. PubMed PMC

Milgroom M.G., Cortesi P. Biological control of chestnut blight with hypovirulence: A critical analysis. Annual Review of Phytopathology. 2004;42:311–338. PubMed

Morris T.J., Dodds J.A. Isolation and analysis of double- stranded-RNA from virus infected plant and fungal tissue. Phytopathology. 1979;69:854–858.

Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Molecular Biology and Evolution. 1986;3:418–426. PubMed

Nibert M.L., Ghabrial S.A., Maiss E., Lesker T., Vainio E., Jiang D., Suzuki N. Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Research. 2014;188:128–141. PubMed

Nuss D.L. Hypovirulence: mycoviruses at the fungal-plant interface. Natural Reviews Microbiology. 2005;3:632–642. PubMed

Nuss D.L. Mycoviruses, RNA silencing, and viral RNA recombination. Advances in Virus Research. 2011;80:25–48. PubMed PMC

Phan T.G., Okitsu S., Niwat Maneekarn A., Ushijima1 H. Evidence of recombination and genetic diversity in southern rice black-streaked dwarf virus. Journal of General Virology. 2007;81:10188.

Pearson M.N., Beever R.E., Boine B., Arthur K. Mycoviruses of filamentous fungi and their relevance to plant pathology. Molecular Plant Pathology. 2009;10:115–128. PubMed PMC

Polashock J.J., Bedker P.J., Hillman B.I. Movement of a small mitochondrial double-stranded RNA element of Cryphonectria parasitica: ascospore inheritance and implications for mitochondrial recombination. Molecular & General Genetics. 1997;256:566–571. PubMed

Romeralo C., Botella L., Santamaria O., Diez J. Effect of putative mitoviruses on in vitro growth of Gremmeniella abietina isolates under different laboratory conditions. Forest Systems. 2012;21:515–525.

Sabanadzovic S., Valverde R.A., Brown J.K., Martin R.R., Tzanetakis I.E. Southern tomato virus: The link between the families Totiviridae and Partitiviridae. Virus Research. 2009;140:130–137. PubMed

Santamaria O., Alves-Santos F.M., Diez J.J. Genetic characterization of Gremmeniella abietina var. abietina isolates from Spain. Plant Pathology. 2005;54:331–338.

Skilling D.D., Schneider B.S., Sullivan J.A. Scleroderris canker on Austrian and ponderosa pine in New York. Plant Disease Reports. 1977;61:707–708.

Sztuba-Solińska J., Urbanowicz A., Figlerowicz M., Bujarski J.J. RNA-RNA recombination in plant virus replication and evolution. Annual Review of Phytopathology. 2011;49:415–443. PubMed

Sun Q., Choi G.H., Nuss D.L. A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:17927–17932. PubMed PMC

Suzuki Y., Gojobori T., Nakagomi O. Intragenic recombinations in rotaviruses. FEBS Letters. 1998;427:183–187. PubMed

Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using Maximum Likelihood, Evolutionary distance, and Maximum Parsimony methods. Molecular Biology and Evolution. 2011;28:2731–2739. PubMed PMC

Tavantzis S. Partitiviruses of fungi. In: Mahy B.W.J., Van Regenmortel M.H.V., editors. Desk Encyclopedia of Plant and Fungal Virology. Elsevier; Oxford, United Kingdom: 2010. pp. 547–552.

Tuomivirta T.T., Uotila A., Hantula J. Two independent doubled- stranded RNA patterns occur in the Finnish Gremmeniella abietina var. abietina type A. Forest Pathology. 2002;32:197–205.

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. Archives of Virology. 2003;148:2293–2305. PubMed

Tuomivirta T.T., Hantula J. Gremmeniella abietina mitochondrial RNA virus S1 is phylogenetically related to the members of the genus Mitovirus. Archives of Virology. 2003;148:2429–2436. PubMed

Tuomivirta T.T., Hantula J. Three unrelated viruses occur in a single isolate of Gremmeniella abietina var. abietina type A. Virus Research. 2005;110:31–39. PubMed

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. Journal of General Virology. 2010;90:2299–2305. PubMed

Uotila A. The effect of climatic factors on the occurrence of Scleroderris canker. Folia Forestalia. 1988;721:1–23.

Uotila A. Mating system and apothecia production in Gremmeniella abietina. European Journal of Forest Pathology. 1992;22:410–417.

Uotila A., Hantula J., Vaatanen A.K., Hamelin R. Hybridization between two biotypes of Gremmeniella abietina var. abietina in artificial pairings. Forest Pathology. 2000;30:211–219.

Uotila A., Hantula J. Proceeding of IUFRO 2013 WP 7.02.02 Foliage, shoot and stems diseases. Brno and Cerna Hora; Czech Republic: 2012. The Gremmeniella spp. taxonomy- types, races or species? p. 53.

Vainio E.J., Korhonen K., Tuomivirta T.T., Hantula J. A novel putative partitivirus of the saprotrophic fungus Heterobasidion ecrustosum infects pathogenic species of the Heterobasidion annosum complex. Fungal Biology. 2010;114:955–965. PubMed

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 Biology. 2011;115:1234–1243. PubMed

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. PubMed

Vainio E.J., Piri T., Hantula J. Virus community dynamics in the conifer pathogenic fungus Heterobasidion parviporum following an artificial introduction of a partitivirus. Microbial Ecology. 2012;65:28–38. PubMed

Voth P.D., Mairura L., Lockhart B.E., May G. Phylogeography of Ustilago maydis virus H1 in the USA and Mexico. Journal of General Virology. 2006;87:3433–3441. PubMed

Wulff S., Walheim M. Swedish University of Agricultural Sciences (SLU), Department of Forest Resource Management and Geomatics; Umeå: 2003. Gremmeniella abietina: uppträdande i Sverige. Resultat från Riksskogstaxeringen och skogsskadeinventeringen 2002; pp. 1–6.

Zhang X., Nuss D.L. A host dicer is required for defective viral RNA production and recombinant virus vector RNA instability for a positive sense RNA virus. Proceedings of the National Academy of Sciences of the United States of America. 2008;105:16749–16754. PubMed PMC

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