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Changes in the composition of the RNA virome mark evolutionary transitions in green plants

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Changes in the composition of the RNA virome mark evolutionary transitions in green plants

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dc.contributor.author Mushegian, Arcady es_ES
dc.contributor.author Shipunov, Alexey es_ES
dc.contributor.author Elena Fito, Santiago Fco es_ES
dc.date.accessioned 2017-05-05T12:16:32Z
dc.date.available 2017-05-05T12:16:32Z
dc.date.issued 2016-08-15
dc.identifier.issn 1741-7007
dc.identifier.uri http://hdl.handle.net/10251/80675
dc.description.abstract Background: The known plant viruses mostly infect angiosperm hosts and have RNA or small DNA genomes. The only other lineage of green plants with a relatively well-studied virome, unicellular chlorophyte algae, is mostly infected by viruses with large DNA genomes. Thus RNA viruses and small DNA viruses seem to completely displace large DNA virus genomes in late branching angiosperms. To understand better the expansion of RNA viruses in the taxonomic span between algae and angiosperms, we analyzed the transcriptomes of 66 non-angiosperm plants characterized by the 1000 Plants Genomes Project. Results: We found homologs of virus RNA-dependent RNA polymerases in 28 non-angiosperm plant species, including algae, mosses, liverworts (Marchantiophyta), hornworts (Anthocerotophyta), lycophytes, a horsetail Equisetum, and gymnosperms. Polymerase genes in algae were most closely related to homologs from double-stranded RNA viruses leading latent or persistent lifestyles. Land plants, in addition, contained polymerases close to the homologs from single-stranded RNA viruses of angiosperms, capable of productive infection and systemic spread. For several polymerases, a cognate capsid protein was found in the same library. Another virus hallmark gene family, encoding the 30 K movement proteins, was found in lycophytes and monilophytes but not in mosses or algae. Conclusions: The broadened repertoire of RNA viruses suggests that colonization of land and growth in anatomical complexity in land plants coincided with the acquisition of novel sets of viruses with different strategies of infection and reproduction. es_ES
dc.description.sponsorship We thank the colleagues at the 1000 Plant Genomes Project for helping us to access the transcriptomes used in this study via the iPlant Collaborative. We are grateful to Javier Forment (IBMCP-CSIC), Vincent Lefort (PhyML), and the E-Biothon team (E-Biothon platform is supported by CNRS, IBM, INRIA, l'Institut Francais de Bioinformatique and SysFera) for expert help with high-performance computing; to Yuri Wolf, Jan Kreuze, Eddie Holmes, and Mang Shi for sharing sequence data and alignments; to Sejo Sabanadzovic, Jan Kreuze, and the anonymous reviewers for helpful virtual discussions and critical remarks; and to Natalia Mushegian for technical assistance. SFF was supported by grants BFU2015-65037P from Spain Ministry of Economy and Competitiveness and PROMETEOII/2014/021 from Generalitat Valenciana. ARM is a Program Director at the US National Science Foundation (NSF); his work on this project was supported by the NSF Independent Research and Development Program, but the statements and opinions expressed herein are made in the personal capacity and do not constitute the endorsement by NSF or the government of the United States. en_EN
dc.language Inglés es_ES
dc.publisher BioMed Central es_ES
dc.relation.ispartof BMC Biology es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject Evolutionary transitions es_ES
dc.subject In silico virus discovery es_ES
dc.subject Metagenomics es_ES
dc.subject Plant evolution es_ES
dc.subject Transcriptome es_ES
dc.subject Virus macroevolution es_ES
dc.title Changes in the composition of the RNA virome mark evolutionary transitions in green plants es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1186/s12915-016-0288-8
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BFU2015-65037-P/ES/EVOLUCION DE VIRUS EN HUESPEDES CON SUSCEPTIBILIDAD VARIABLE: CONSECUENCIAS EN EFICACIA Y VIRULENCIA DE CAMBIOS EN LAS REDES INTERACTOMICAS DE PROTEINAS VIRUS-HUESPED/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEOII%2F2014%2F021/ES/Comparative systems biology of host-virus interactions/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Mushegian, A.; Shipunov, A.; Elena Fito, SF. (2016). Changes in the composition of the RNA virome mark evolutionary transitions in green plants. BMC Biology. 14(68):1-14. https://doi.org/10.1186/s12915-016-0288-8 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion http://dx.doi.org/10.1186/s12915-016-0288-8 es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 14 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 14 es_ES
dc.description.issue 68 es_ES
dc.relation.senia 323456 es_ES
dc.identifier.pmid 27524491 en_EN
dc.identifier.pmcid PMC4983792 en_EN
dc.contributor.funder Generalitat Valenciana es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.contributor.funder Institut Français de Bioinformatique es_ES
dc.contributor.funder Centre National de la Recherche Scientifique, Francia es_ES
dc.contributor.funder International Business Machines Corporation es_ES
dc.contributor.funder National Science Foundation, EEUU
dc.description.references Roossinck MJ. Plant virus metagenomics: biodiversity and ecology. Annu Rev Genet. 2012;46:357–67. es_ES
dc.description.references Koonin EV, Dolja VV, Krupovic M. Origins and evolution of viruses of eukaryotes: The ultimate modularity. Virology. 2015;479-480:2–25. es_ES
dc.description.references Yamada T, Onimatsu H, Van Etten JL. Chlorella viruses. Adv Virus Res. 2006;66:293–336. es_ES
dc.description.references Van Etten JL, Dunigan DD. Chloroviruses: not your everyday plant virus. Trends Plant Sci. 2012;17:1–8. es_ES
dc.description.references Zhang T, Jiang Y, Dong W. A novel monopartite dsRNA virus isolated from the phytopathogenic fungus Ustilaginoidea virens and ancestrally related to a mitochondria-associated dsRNA in the green alga Bryopsis. Virology. 2014;462:227–35. es_ES
dc.description.references Wilson WH, Van Etten JL, Allen MJ. The Phycodnaviridae: the story of how tiny giants rule the world. Curr Top Microbiol Immunol. 2009;328:1–42. es_ES
dc.description.references Iyer LM, Balaji S, Koonin EV, Aravind L. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res. 2006;117:156–84. es_ES
dc.description.references Colson P, De Lamballerie X, Yutin N, Asgari S, Bigot Y, Bideshi DK, et al. “Megavirales”, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch Virol. 2013;158:2517–21. es_ES
dc.description.references Gibbs AJ, Torronen M, Mackenzie AM, Wood 2nd JT, Amstrong JS, Kondo H, et al. The enigmatic genome of Chara australis virus. J Gen Virol. 2011;92:2679–90. es_ES
dc.description.references Valverde RA, Sabanadzovic S. A novel plant virus with unique properties infecting Japanese holly fern. J Gen Virol. 2009;90:42–9. es_ES
dc.description.references Han SS, Karasev AV, Ieki H, Iwanami T. Nucleotide sequence and taxonomy of Cycas necrotic stunt virus. Brief report. Arch Virol. 2002;147:2207–14. es_ES
dc.description.references Lockhart B, Fetzer JL, Olszewski NE. Preliminary characterization of Cycad leaf necrosis virus, the first badnavirus identified in cycads. Phytopathology. 2006;96:S70. es_ES
dc.description.references Mushegian AR, Elena SF. Evolution of plant virus movement proteins from the 30 K superfamily and of their homologs integrated in plant genomes. Virology. 2015;476:304–15. es_ES
dc.description.references Maumus F, Epert A, Nogué F, Blanc G. Plant genomes enclose footprints of past infections by giant virus relatives. Nat Commun. 2014;5:4268. es_ES
dc.description.references Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, et al. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci USA. 2014;111:E4859–68. es_ES
dc.description.references Merchant N, Lyons E, Goff S, Vaughn M, Ware D, Micklos D, et al. The iPlant collaborative: cyberinfrastructure for enabling data to discovery for the life sciences. PLoS Biol. 2016;14:e1002342. es_ES
dc.description.references Becker B, Marin B. Streptophyte algae and the origin of embryophytes. Ann Bot. 2009;103:999–1004. es_ES
dc.description.references Koonin EV, Dolja VV. A virocentric perspective on the evolution of life. Curr Op Virol. 2013;3:546–57. es_ES
dc.description.references Matasci N, Huang LH, Yan Z, Carpenter EJ, Wickett NJ, Mirarab S, et al. Data access for the 1000 plants (1KP) project. Gigascience. 2014;3:17. es_ES
dc.description.references Makarova KS, Aravind L, Grishin NV, Rogozin IB, Koonin EV. A DNA repair system specific for thermophilic Archaea and bacteria predicted by genomic context analysis. Nucleic Acids Res. 2002;30:482–96. es_ES
dc.description.references Majumdar I, Kinch LN, Grishin NV. A database of domain definitions for proteins with complex interdomain geometry. PLoS ONE. 2009;4:e5084. es_ES
dc.description.references Černý J, Černá Bolfíková B, Zanotto PMA, Grubhoffer L, Růžek D. A deep phylogeny of viral and cellular right-hand polymerases. Infec Genet Evol. 2015;36:275–86. es_ES
dc.description.references Iyer LM, Koonin EV, Aravind L. Evolutionary connection between the catalytic subunits of DNA-dependent RNA polymerases and eukaryotic RNA-dependent RNA polymerases and the origin of RNA polymerases. BMC Struct Biol. 2003;3:1. es_ES
dc.description.references Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402. es_ES
dc.description.references Koga R, Horiuchi H, Fukuhara T. Double-stranded RNA replicons associated with chloroplasts of a green alga, Bryopsis cinicola. Plant Mol Biol. 2003;51:991–9. es_ES
dc.description.references Jablonski SA, Morrow CD. Mutation of the aspartic acid residues of the GDD sequence motif of poliovirus RNA-dependent RNA polymerase results in enzymes with altered metal ion requirements for activity. J Virol. 1995;69:1532–9. es_ES
dc.description.references Morin B, Whelan SPJ. La protéine L des Mononegavirales. Virologie. 2012;16:258–68. es_ES
dc.description.references Liang B, Li Z, Jenni S, Rahmeh AA, Morin BM, Grant T, et al. Structure of the L protein of Vesicular stomatitis virus from electron cryomicroscopy. Cell. 2015;162:314–27. es_ES
dc.description.references Chabannes M, Iskra-Caruana ML. Endogenous pararetroviruses – a reservoir of virus infection in plants. Curr Opin Virol. 2013;3:615–20. es_ES
dc.description.references Bousios A, Darzentas N. Sirevirus LTR retrotransposons: phylogenetic misconceptions in the plant world. Mob DNA. 2013;4:9. es_ES
dc.description.references Bertsch C, Beuve M, Dolja VV, Wirth M, Pelsy F, Herrbach E, et al. Retention of the virus-derived sequences in the nuclear genome of grapevine as a potential pathway to virus resistance. Biol Direct. 2009;4:21. es_ES
dc.description.references Roossinck MJ. Lifestyle of plant viruses. Philos Trans R Soc B. 2010;365:1899–905. es_ES
dc.description.references Nibert ML, Ghabrial SA, Maiss E, Lesker T, Vainio EJ, Jiang D, et al. Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res. 2014;188:128–41. es_ES
dc.description.references Koonin EV, Wolf YI, Nagasaki K, Dolja VV. The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol. 2008;6:925–39. es_ES
dc.description.references Poch O, Sauvaget I, Delarue M, Tordo N. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J. 1989;8:3867–74. es_ES
dc.description.references Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21. es_ES
dc.description.references Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016;44(W1):W242. es_ES
dc.description.references Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife. 2015;29:4. es_ES
dc.description.references Yutin N, Wolf YI, Raoult D, Koonin EV. Eukaryotic large nucleo-cytoplasmic DNA viruses: clusters of orthologous genes and reconstruction of viral genome evolution. Virol J. 2009;6:223. es_ES
dc.description.references Liu H, Fu Y, Xie J, Cheng J, Ghabrial SA, Li G, et al. Evolutionary genomics of mycovirus-related dsRNA viruses reveals cross-family horizontal gene transfer and evolution of diverse viral lineages. BMC Evol Biol. 2012;12:91. es_ES
dc.description.references Atsatt PR, Whiteside MD. Novel symbiotic protoplasts formed by endophytic fungi explain their hidden existence, lifestyle switching, and diversity within the plant kingdom. PLoS ONE. 2014;9:e95266. es_ES
dc.description.references Hom EF, Murray AW. Plant-fungal ecology. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science. 2014;345:94–8. es_ES
dc.description.references Magallón S, Hilu KW, Quandt D. Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. Am J Bot. 2013;100:556–73. es_ES
dc.description.references Johnson MT, Carpenter EJ, Tian Z, Bruskiewich R, Burris JN, Carrigan CT, et al. Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLoS One. 2012;7:e50226. es_ES
dc.description.references Kreuze J. siRNA deep sequencing and assembly: piecing together viral infections. In: Gullino ML, Bonants PJM, editors. Detection and diagnostics of plant pathogens. Dordrecht: Springer; 2014. p. 21–38. es_ES
dc.description.references Chávez Montes RA, de Fátima R-CF, De Paoli E, Accerbi M, Rymarquis LA, Mahalingam G, et al. Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat Commun. 2014;5:3722. es_ES
dc.description.references Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI’s conserved domain database. Nucl Acids Res. 2015;43:D222–6. es_ES
dc.description.references Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004;5:113. es_ES
dc.description.references Söding J, Biegert A, Lupas AN. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2015;33:W244–8. es_ES
dc.description.references Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25(7):1307–20. es_ES
dc.description.references Daydé M, Depardon B, Franc A, Gibrat JF, Guillier R, Karami Y, Sutter F, Taddese B, Chabbert M, Thérond S. E-Biothon: an experimental platform for bioinformatics. 2015 Computer Science and Information Technologies (CSIT) 2015;1-4. es_ES
dc.description.references Okuno K, Hama T, Takeshita M, Furuya N, Takanami Y. New potyvirus isolated from Cryptotaenia japonica. J Gen Plant Pathol. 2003;69:138–42. es_ES


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