We explored the virome of the "Phytophthora palustris complex", a group of aquatic specialists geographically limited to Southeast and East Asia, the native origin of many destructive invasive forest Phytophthora spp. Based on high-throughput sequencing (RNAseq) of 112 isolates of "P. palustris" collected from rivers, mangroves, and ponds, and natural forests in subtropical and tropical areas in Indonesia, Taiwan, and Japan, 52 putative viruses were identified, which, to varying degrees, were phylogenetically related to the families Botybirnaviridae, Narnaviridae, Tombusviridae, and Totiviridae, and the order Bunyavirales. The prevalence of all viruses in their hosts was investigated and confirmed by RT-PCR. The rich virus composition, high abundance, and distribution discovered in our study indicate that viruses are naturally infecting taxa from the "P. palustris complex" in their natural niche, and that they are predominant members of the host cellular environment. Certain Indonesian localities are the viruses' hotspots and particular "P. palustris" isolates show complex multiviral infections. This study defines the first bi-segmented bunya-like virus together with the first tombus-like and botybirna-like viruses in the genus Phytophthora and provides insights into the spread and evolution of RNA viruses in the natural populations of an oomycete species.

Department of Genetics and Agrobiotechnology Faculty of Agriculture and Technology University of South Bohemia in České Budějovice Na Sádkách 1780 370 05 České Budějovice Czech Republic

Phytophthora Research Centre Department of Forest Protection and Wildlife Management Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 3 613 00 Brno Czech Republic

Zobrazit více v PubMed

Brasier C.M. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 2008;57:792–808. doi: 10.1111/j.1365-3059.2008.01886.x. DOI

Santini A., Ghelardini L., De Pace C., Desprez-Loustau M.L., Capretti P., Chandelier A., Cech T., Chira D., Diamandis S., Gaitniekis T., et al. Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytol. 2013;197:238–250. doi: 10.1111/j.1469-8137.2012.04364.x. PubMed DOI

Hantula J., Müller M.M., Uusivuori J. International plant trade associated risks: Laissez-faire or novel solutions. Environ. Sci. Policy. 2014;37:158–160. doi: 10.1016/j.envsci.2013.09.011. DOI

Jung T., Orlikowski L., Henricot B., Abad-Campos P., Aday A.G., Aguín Casal O., Bakonyi J., Cacciola S.O., Cech T., Chavarriaga D., et al. Widespread Phytophthora infestations in European nurseries put forest, semi-natural and horticultural ecosystems at high risk of Phytophthora diseases. For. Pathol. 2016;46:134–163. doi: 10.1111/efp.12239. DOI

Boyd I.L., Freer-Smith P.H., Gilligan C.A., Godfray H.C.J. The consequence of tree pests and diseases for ecosystem services. Science. 2013;342:1235773. doi: 10.1126/science.1235773. PubMed DOI

Jung T., Pérez-Sierra A., Durán A., Jung M.H., Balci Y., Scanu B. Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia. 2018;40:182. doi: 10.3767/persoonia.2018.40.08. PubMed DOI PMC

Sakai A.K., Allendorf F.W., Holt J.S., Lodge D.M., Molofsky J., With K.A., Baughman S., Cabin R.J., Cohen J.E., Ellstrand N.C., et al. The population biology of invasive species. Annu. Rev. Ecol. Syst. 2001;32:305–332. doi: 10.1146/annurev.ecolsys.32.081501.114037. DOI

Roderick G.K., Navajas M. Genes in new environments: Genetics and evolution in biological control. Nat. Rev. Genet. 2003;4:889–899. doi: 10.1038/nrg1201. PubMed DOI

Mitchell C.E., Power A.O. Release of invasive plants from fungal and viral pathogens. Nature. 2003;421:625–627. doi: 10.1038/nature01317. PubMed DOI

Derelle R., López-García P., Timpano H., Moreira D. A phylogenomic framework to study the diversity and evolution of Stramenopiles (=Heterokonts) Mol. Biol. Evol. 2016;33:2890–2898. doi: 10.1093/molbev/msw168. PubMed DOI PMC

Richards T.A., Dacks J.B., Jenkinson J.M., Thornton C.R., Talbot N.J. Evolution of filamentous plant pathogens: Gene exchange across eukaryotic kingdoms. Curr. Biol. 2006;16:1857–1864. doi: 10.1016/j.cub.2006.07.052. PubMed DOI

Brasier C.M., Vettraino A.M., Chang T.T., Vannini A. Phytophthora lateralis discovered in an old growth Chamaecyparis forest in Taiwan. Plant Pathol. 2010;59:595–603. doi: 10.1111/j.1365-3059.2010.02278.x. DOI

Brasier C.M., Franceschini S., Vettraino A.M., Hansen E.M., Green S., Robin C., Webber J.F., Vannini A. Four phenotypically and phylogenetically distinct lineages in Phytophthora lateralis. Fungal Biol. 2012;116:1232–1249. doi: 10.1016/j.funbio.2012.10.002. PubMed DOI

Jung T., Chang T.T., Bakonyi J., Seress D., Pérez-Sierra A., Yang X., Hong C., Scanu B., Fu C.H., Hsueh K.L., et al. Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathol. 2017;66:194–211. doi: 10.1111/ppa.12564. DOI

Jung T., Scanu B., Brasier C.M., Webber J., Milenković I., Corcobado T., Tomšovský M., Pánek M., Bakonyi J., Maia C., et al. A survey in natural forest ecosystems of Vietnam reveals high diversity of both new and described Phytophthora taxa including P. ramorum. Forests. 2020;11:93. doi: 10.3390/f11010093. DOI

Jung T., Jung M.H., Webber J.F., Kageyama K., Hieno A., Masuya H., Uematsu S., Pérez-Sierra A., Harris A.R., Forster J., et al. The destructive tree pathogen Phytophthora ramorum originates from the laurosilva forests of East Asia. J. Fungi. 2021;7:226. doi: 10.3390/jof7030226. PubMed DOI PMC

Jung T., Milenković I., Corcobado T., Májek T., Janoušek J., Kudláček T., Tomšovský M., Nagy Z., Durán A., Tarigan M., et al. Extensive morphological and behavioural diversity among fourteen new and seven described species in Phytophthora Clade 10 and its evolutionary implications. Persoonia. 2022;49:1–57. doi: 10.3767/persoonia.2022.49.01. PubMed DOI PMC

Gower D.J., Johnson K.G., Richardson J.E., Rosen B.R., Ruber L.W.S. Biotic Evolution and Environmental Change in Southeast Asia. Cambridge University Press; Cambrigde, UK: 2012.

Prospero S., Botella L., Santini A., Robin C. Biological control of emerging forest diseases: How can we move from dreams to reality? For. Ecol. Manag. 2021;496:119377. doi: 10.1016/j.foreco.2021.119377. DOI

Rigling D., Prospero S. Cryphonectria parasitica, the causal agent of chestnut blight: Invasion history, population biology and disease control. Mol. Plant Pathol. 2018;19:7–20. doi: 10.1111/mpp.12542. PubMed DOI PMC

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

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

Lefeuvre P., Martin D.P., Elena S.F., Shepherd D.N., Roumagnac P., Varsani A. Evolution and ecology of plant viruses. Nat. Rev. Microbiol. 2019;17:632–644. doi: 10.1038/s41579-019-0232-3. PubMed DOI

Poisot T., Stouffer D.B., Gravel D. Beyond species: Why ecological interaction networks vary through space and time. Oikos. 2015;124:243–251. doi: 10.1111/oik.01719. DOI

Schoelz J.E., Stewart L.R. The Role of Viruses in the Phytobiome. Annu. Rev. Virol. 2018;5:93–111. doi: 10.1146/annurev-virology-092917-043421. PubMed DOI

French R.K., Holmes E.C. An ecosystems perspective on virus evolution and emergence. Trends Microbiol. 2020;28:165–175. doi: 10.1016/j.tim.2019.10.010. PubMed DOI

Ihrmark K., Johannesson H., Stenström E., Stenlid J. Transmission of double-stranded RNA in Heterobasidion annosum. Fungal Genet. Biol. 2022;36:147–154. doi: 10.1016/S1087-1845(02)00011-7. PubMed DOI

Ihrmark K., Stenström E., Stenlid J. Double-stranded RNA transmission through basidiospores of Heterobasidion annosum. Mycol. Res. 2004;108:149–153. doi: 10.1017/S0953756203008839. PubMed 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

Voth P.D., Mairura L., Lockhart B.E., May G. Phylogeography of Ustilago maydis virus H1 in the USA and Mexico. J. Gen. Virol. 2006;87:3433–3441. doi: 10.1099/vir.0.82149-0. 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

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

Botella L., Jung T. Multiple viral infections detected in Phytophthora condilina by total and small RNA sequencing. Viruses. 2021;13:620. doi: 10.3390/v13040620. PubMed DOI PMC

Cai G., Hillman B.I. Phytophthora Viruses. 1st ed. Volume 86. Elsevier Inc; Amsterdam, The Netherlands: 2013.

Hacker C.V., Brasier C.M., Buck K.W. A double-stranded RNA from a Phytophthora species is related to the plant endornaviruses and contains a putative UDP glycosyltransferase gene. J. Gen. Virol. 2005;86:1561–1570. doi: 10.1099/vir.0.80808-0. PubMed DOI

Kozlakidis Z., Brown N.A., Jamal A., Phoon X., Coutts R.H.A. Incidence of endornaviruses in Phytophthora taxon douglasfir and Phytophthora ramorum. Virus Genes. 2010;40:130–134. doi: 10.1007/s11262-009-0421-7. PubMed DOI

Poimala A., Parikka P., Hantula J., Vainio E.J. Viral diversity in Phytophthora cactorum population infecting strawberry. Environ. Microbiol. 2021;23:5200–5221. doi: 10.1111/1462-2920.15519. PubMed DOI

Uchida K., Sakuta K., Ito A., Takahashi Y., Katayama Y., Omatsu T., Mizutani T., Arie T., Komatsu K., Fukuhara T., et al. Two novel endornaviruses co-infecting a phytophthora pathogen of Asparagus officinalis modulate the developmental stages and fungicide sensitivities of the host oomycete. Front. Microbiol. 2021;12:633502. doi: 10.3389/fmicb.2021.633502. PubMed DOI PMC

Xu Z., Khalifa M.E., Frampton R.A., Smith G.R., McDougal R.L., Macdiarmid R.M., Kalamorz F. Characterization of a novel double-stranded RNA virus from Phytophthora pluvialis in New Zealand. Viruses. 2022;14:247. doi: 10.3390/v14020247. PubMed DOI PMC

Raco M., Vainio E., Sutela S., Eichmeier A., Hakalová E., Jung T., Botella L. High diversity of novel viruses in the tree pathogen Phytophthora castaneae revealed by high-throughput sequencing of total and small RNA. Front. Microbiol. 2022;13:911474. doi: 10.3389/fmicb.2022.911474. PubMed DOI PMC

Hannat S., Pontarotti P., Colson P., Kuhn M.L., Galiana E., La Scola B., Aherfi S., Panabières F. Diverse trajectories drive the expression of a giant virus in the oomycete plant pathogen Phytophthora parasitica. Front. Microbiol. 2021;12:1–13. doi: 10.3389/fmicb.2021.662762. PubMed DOI PMC

Grasse W., Spring O. Occurrence and genetic diversity of the Plasmopara halstedii virus in sunflower downy mildew populations of the world. Fungal Biol. 2015;119:170–178. doi: 10.1016/j.funbio.2014.12.004. PubMed DOI

Chiapello M., Rodríguez-Romero J., Nerva L., Forgia M., Chitarra W., Ayllón M.A., Turina M. Putative new plant viruses associated with Plasmopara viticola -infected grapevine samples. Ann. Appl. Biol. 2020;176:180–191. doi: 10.1111/aab.12563. DOI

Shiba K., Hatta C., Sasai S., Tojo M., Ohki T.S., Mochizuki T. Genome sequence of a novel partitivirus identified from the oomycete Pythium nunn. Arch. Virol. 2018;163:2561–2563. doi: 10.1007/s00705-018-3880-0. PubMed DOI

Sasai S., Tamura K., Tojo M., Herrero M.L., Hoshino T., Ohki S.T., Mochizuki T. A novel non-segmented double-stranded RNA virus from an Arctic isolate of Pythium polare. Virology. 2018;522:234–243. doi: 10.1016/j.virol.2018.07.012. PubMed DOI

Botella L., Janoušek J., Maia C., Jung M.H., Raco M., Jung T. Marine oomycetes of the genus Halophytophthora harbor viruses related to bunyaviruses. Front. Microbiol. 2020;11:1–13. doi: 10.3389/fmicb.2020.01467. PubMed DOI PMC

Fukunishi M., Sasai S., Tojo M., Mochizuki T. Novel fusari- and toti-like viruses, with probable different origins, in the plant pathogenic oomycete Globisporangium ultimum. Viruses. 2021;13:1931. doi: 10.3390/v13101931. PubMed DOI PMC

Chomczynski P., Wilfinger W., Kennedy A., Rymaszewski M., Mackey K. RNAzol® RT: A new single-step method for isolation of RNA. Nat. Methods. 2010;7:4–5. doi: 10.1038/nmeth.f.315. DOI

Brister J.R., Ako-Adjei D., Bao Y., Blinkova O. NCBI viral genomes resource. Nucleic Acids Res. 2015;43:D571–D577. doi: 10.1093/nar/gku1207. PubMed DOI PMC

Stamatakis A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–2690. doi: 10.1093/bioinformatics/btl446. PubMed DOI

Miller M.A., Pfeiffer W., Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees; Proceedings of the Gateway Computing Environments Workshop (GCE); New Orleans, LA, USA. 14 November 2010; pp. 1–8.

R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2021. [(accessed on 28 August 2022)]. Available online: https://www.R-project.org/

Muller R., Poch O., Delarue M., Bishop D.H.L., Bouloy M. Rift valley fever virus L segment: Correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J. Gen. Virol. 1994;75:1345–1352. doi: 10.1099/0022-1317-75-6-1345. PubMed DOI

Wille M., Eden J., Shi M., Klaassen M., Hurt A.C., Holmes E.C. Virus–virus interactions and host ecology are associated with RNA virome structure in wild birds. Mol. Ecol. 2018;27:5263–5278. doi: 10.1111/mec.14918. PubMed DOI PMC

Yokoi T., Yamashita S., Hibi T. The nucleotide sequence and genome organization of Sclerophthora macrospora virus A. Virology. 2003;311:394–399. doi: 10.1016/S0042-6822(03)00183-1. PubMed DOI

Starr E.P., Nuccio E.E., Pett-Ridge J., Banfield J.F., Firestone M.K. Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil. Proc. Natl. Acad. Sci. USA. 2019;116:25900–25908. doi: 10.1073/pnas.1908291116. PubMed DOI PMC

Preisig O., Moleleki N., Smit W.A., Wingfield B.D., Wingfield M.J. A noval RNA mycovirus in a hypovirulent isolate of the plant pathogen Diaporthe ambigua. J. Gen. Virol. 2000;81:3107–3114. doi: 10.1099/0022-1317-81-12-3107. PubMed DOI

Kondo H., Botella L., Suzuki N. Mycovirus Diversity and Evolution Revealed/Inferred from Recent Studies. Annu. Rev. Phytopathol. 2022;60:1–30. doi: 10.1146/annurev-phyto-021621-122122. PubMed DOI

Zhou L., Li X., Kotta-Loizou I., Dong K., Li S., Ni D., Hong N., Wang G., Xu W. A mycovirus modulates the endophytic and pathogenic traits of a plant associated fungus. ISME J. 2021;15:1893–1906. doi: 10.1038/s41396-021-00892-3. PubMed DOI PMC

Forgia M., Isgandarli E., Aghayeva D.N., Huseynova I., Turina M. Virome characterization of Cryphonectria parasitica isolates from Azerbaijan unveiled a new mymonavirus and a putative new RNA virus unrelated to described viral sequences. Virology. 2021;553:51–61. doi: 10.1016/j.virol.2020.10.008. PubMed DOI

Chiapello M., Rodríguez-Romero J., Ayllón M.A., Turina M. Analysis of the virome associated to grapevine downy mildew lesions reveals new mycovirus lineages. Virus Evol. 2020;6:1–18. doi: 10.1093/ve/veaa058. PubMed DOI PMC

Jones R.A.C. Plant and insect viruses in managed and natural environments: Novel and neglected transmission pathways. Adv. Virus Res. 2018;101:149–187. PubMed

Issaka S., Traoré O., Longué R.D.S., Pinel-Galzi A., Gill M.S., Dellicour S., Bastide P., Guindon S., Hébrard E., Dugué M.J., et al. Rivers and landscape ecology of a plant virus, Rice yellow mottle virus along the Niger Valley. Virus Evol. 2021;7:veab072. doi: 10.1093/ve/veab072. PubMed DOI PMC

Büttner C., Jacobi V., Koenig R. Isolation of Carnation Italian Ringspot Virus from a creek in a forested area south west of Bonn. J. Phytopathol. 1987;118:131–134. doi: 10.1111/j.1439-0434.1987.tb00441.x. DOI

Culley A.I., Lang A.S., Suttla C.A. Metagenomic analysis of coastal RNA virus communities. Science. 2006;312:1795–1798. doi: 10.1126/science.1127404. PubMed DOI

Shi M., Lin X.D., Tian J.H., Chen L.J., Chen X., Li C.X., Qin X.C., Li J., Cao J.P., Eden J.S., et al. Redefining the invertebrate RNA virosphere. Nature. 2016;540:539–543. doi: 10.1038/nature20167. PubMed DOI

Zhang Y.Y., Chen Y., Wei X., Cui J. Viromes in marine ecosystems reveal remarkable invertebrate RNA virus diversity. Sci. China Life Sci. 2021;2021:1–12. doi: 10.1007/s11427-020-1936-2. PubMed DOI

Li H., Roossinck M.J. Genetic bottlenecks reduce population variation in an experimental RNA virus population. Society. 2004;78:10582–10587. doi: 10.1128/JVI.78.19.10582-10587.2004. PubMed DOI PMC

Vives M.C., Rubio L., Galipienso L., Navarro L., Moreno P., Guerri J. Low genetic variation between isolates of Citrus leaf blotch virus from different host species and of different geographical origins. J. Gen. Virol. 2002;83:2587–2591. doi: 10.1099/0022-1317-83-10-2587. PubMed DOI

Barr J.N., Fearns R. How RNA viruses maintain their genome integrity. J. Gen. Virol. 2010;91:1373–1387. doi: 10.1099/vir.0.020818-0. PubMed DOI

Botella L., Hantula J. Description, Distribution, and Relevance of Viruses of the Forest Pathogen Gremmeniella abietina. Viruses. 2018;10:654. doi: 10.3390/v10110654. PubMed DOI PMC

Wu M., Zhang J., Yang L., Li G. RNA mycoviruses and their role in Botrytis biology. In: Fillinger S., Elad Y., editors. Botrytis—The Fungus, the Pathogen and Its Management in Agricultural Systems. Springer; Cham, Switzerland: 2015. pp. 71–90.

Marzano S.-Y.L., Nelson B.D., Ajayi-Oyetunde O., Bradley C.A., Hughes T.J., Hartman G.L., Eastburn D.M., Domier L.L. Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J. Virol. 2016;90:6846–6863. doi: 10.1128/JVI.00357-16. PubMed DOI PMC

Briese T., Calisher C.H., Higgs S. Viruses of the family Bunyaviridae: Are all available isolates reassortants? Virology. 2013;446:207–216. doi: 10.1016/j.virol.2013.07.030. PubMed DOI

Neriya Y., Morikawa T., Hamamoto K., Noguchi K., Kobayashi T., Suzuki T., Nishigawa H., Natsuaki T. Characterization of tulip streak virus, a novel virus associated with the family Phenuiviridae. J. Gen. Virol. 2021;102:001525. doi: 10.1099/jgv.0.001525. PubMed DOI

Linn Y.H., Fujita M., Sotaro C., Hyodo K., Andika I.B., Suzuki N., Kondo H. Two novel fungal negative-strand RNA viruses related to mymonaviruses and phenuiviruses in the shiitake mushroom (Lentinula edodes) Virology. 2019;533:125–136. doi: 10.1016/j.virol.2019.05.008. PubMed DOI

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. Evol. Appl. 2014;7:580–596. doi: 10.1111/eva.12157. PubMed DOI PMC

Jung T., Stukely M.J.C., Hardy G.E.S.J., White D., Paap T., Dunstan W.A., Burgess T.I. Multiple new Phytophthora species from ITS Clade 6 associated with natural ecosystems in Australia: Evolutionary and ecological implications. Pers. Mol. Phylogeny Evol. Fungi. 2011;26:13–39. doi: 10.3767/003158511X557577. PubMed DOI PMC

Thines M., Choi Y.J. Evolution, diversity, and taxonomy of the Peronosporaceae, with focus on the genus Peronospora. Phytopathology. 2016;106:6–18. doi: 10.1094/PHYTO-05-15-0127-RVW. PubMed DOI

Cai G., Fry W.E., Hillman B.I. PiRV-2 stimulates sporulation in Phytophthora infestans. Virus Res. 2019;271:197674. doi: 10.1016/j.virusres.2019.197674. PubMed DOI

Deakin G., Dobbs E., Bennett J.M., Jones I.M., Grogan H.M., Burton K.S. Multiple viral infections in Agaricus bisporus-Characterisation of 18 unique RNA viruses and 8 ORFans identified by deep sequencing. Sci. Rep. 2017;7:2469. doi: 10.1038/s41598-017-01592-9. PubMed DOI PMC

Schardl C.L., Craven K.D. Interspecific hybridization in plant-associated fungi and oomycetes: A review. Mol. Ecol. 2003;12:2861–2873. doi: 10.1046/j.1365-294X.2003.01965.x. PubMed DOI

Burgess T.I. Molecular characterization of natural hybrids formed between five related indigenous clade 6 Phytophthora species. PLoS ONE. 2015;10:e0134225. doi: 10.1371/journal.pone.0134225. PubMed DOI PMC

Jung T., Jung M.H., Scanu B., Seress D., Kovács G.M., Maia C., Pérez-Sierra A., Chang T.T., Chandelier A., Heungens K., et al. Six new Phytophthora species from ITS clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Pers. Mol. Phylogeny Evol. Fungi. 2017;38:100–135. doi: 10.3767/003158517X693615. PubMed DOI PMC

Dothistroma septosporum and Dothistroma pini, the causal agents of Dothistroma needle blight, are infected by multiple viruses

Diversity and impact of single-stranded RNA viruses in Czech Heterobasidion populations

Sequence and phylogenetic analysis of a novel alphaendornavirus, the first virus described from the oomycete plant pathogen Phytophthora heveae