Experimental evolution of pseudogenization and gene loss in a plant RNA virus
[EN] Viruses have evolved highly streamlined genomes and a variety of mechanisms to compress them, suggesting that genome size is under strong selection. Horizontal gene transfer has, on the other hand, played an important role in virus evolution. However, evolution cannot integrate initially nonfun...
| Autores: | , , , |
|---|---|
| Formato: | artículo |
| Fecha de publicación: | 2014 |
| País: | España |
| Recursos: | Universitat Politècnica de València (UPV) |
| Repositorio: | RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia |
| Idioma: | inglés |
| OAI Identifier: | oai:riunet.upv.es:10251/72658 |
| Acesso em linha: | https://riunet.upv.es/handle/10251/72658 |
| Access Level: | acceso abierto |
| Palavra-chave: | Genome evolution Plant virus Horizontal gene transfer Pseudogenization Fitness Next-generation sequencing |
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España |
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| dc.title.none.fl_str_mv |
Experimental evolution of pseudogenization and gene loss in a plant RNA virus |
| title |
Experimental evolution of pseudogenization and gene loss in a plant RNA virus |
| spellingShingle |
Experimental evolution of pseudogenization and gene loss in a plant RNA virus Zwart, Mark Peter Genome evolution Plant virus Horizontal gene transfer Pseudogenization Fitness Next-generation sequencing |
| title_short |
Experimental evolution of pseudogenization and gene loss in a plant RNA virus |
| title_full |
Experimental evolution of pseudogenization and gene loss in a plant RNA virus |
| title_fullStr |
Experimental evolution of pseudogenization and gene loss in a plant RNA virus |
| title_full_unstemmed |
Experimental evolution of pseudogenization and gene loss in a plant RNA virus |
| title_sort |
Experimental evolution of pseudogenization and gene loss in a plant RNA virus |
| dc.creator.none.fl_str_mv |
Zwart, Mark Peter Willemsen, Anouk Elena Fito, Santiago Fco Daròs, José-Antonio|||0000-0002-6535-2889 |
| author |
Zwart, Mark Peter |
| author_facet |
Zwart, Mark Peter Willemsen, Anouk Elena Fito, Santiago Fco Daròs, José-Antonio|||0000-0002-6535-2889 |
| author_role |
author |
| author2 |
Willemsen, Anouk Elena Fito, Santiago Fco Daròs, José-Antonio|||0000-0002-6535-2889 |
| author2_role |
author author author |
| dc.contributor.none.fl_str_mv |
Instituto Universitario Mixto de Biología Molecular y Celular de Plantas Ministerio de Ciencia e Innovación John Templeton Foundation Ministerio de Economía y Competitividad Repositorio Institucional de la Universitat Politècnica de València Riunet |
| dc.subject.none.fl_str_mv |
Genome evolution Plant virus Horizontal gene transfer Pseudogenization Fitness Next-generation sequencing |
| topic |
Genome evolution Plant virus Horizontal gene transfer Pseudogenization Fitness Next-generation sequencing |
| description |
[EN] Viruses have evolved highly streamlined genomes and a variety of mechanisms to compress them, suggesting that genome size is under strong selection. Horizontal gene transfer has, on the other hand, played an important role in virus evolution. However, evolution cannot integrate initially nonfunctional sequences into the viral genome if they are rapidly purged by selection. Here we report on the experimental evolution of pseudogenization in virus genomes using a plant RNA virus expressing a heterologous gene. When long 9-week passages were performed, the added gene was lost in all lineages, whereas viruses with large genomic deletions were fixed in only two out of ten 3-week lineages and none in 1-week lineages. Illumina next-generation sequencing revealed considerable convergent evolution in the 9- and 3-week lineages with genomic deletions. Genome size was correlated to within-host competitive fitness, although there was no correlation with virus accumulation or virulence. Within-host competitive fitness of the 3-week virus lineages without genomic deletions was higher than for the 1-week lineages. Our results show that the strength of selection for a reduced genome size and the rate of pseudogenization depend on demographic conditions. Moreover, for the 3-week passage condition, we observed increases in within-host fitness, whereas selection was not strong enough to quickly remove the nonfunctional heterologous gene. These results suggest a demographically determined "sweet spot" might exist, where heterologous insertions are not immediately lost while evolution can act to integrate them into the viral genome. |
| publishDate |
2014 |
| dc.date.none.fl_str_mv |
2014 2014-01-01 |
| dc.type.none.fl_str_mv |
journal article http://purl.org/coar/resource_type/c_6501 VoR http://purl.org/coar/version/c_970fb48d4fbd8a85 |
| dc.type.openaire.fl_str_mv |
info:eu-repo/semantics/article |
| format |
article |
| dc.identifier.none.fl_str_mv |
https://riunet.upv.es/handle/10251/72658 |
| url |
https://riunet.upv.es/handle/10251/72658 |
| dc.language.none.fl_str_mv |
Inglés eng |
| language_invalid_str_mv |
Inglés |
| language |
eng |
| dc.relation.none.fl_str_mv |
John Templeton Foundation https://doi.org/10.13039/100000925 22371 Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 BFU2012-30805 EVOLUTIONARY SYSTEMS VIROLOGY: EPISTASIS AND THE RUGGEDNESS OF ADAPTIVE LANDSCAPES, MUTATIONS IN REGULATORY SEQUENCES, AND THE HOST DETERMINANTS OF VIRAL FITNESS Ministerio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 JCI-2011-10379 JCI-2011-10379 Ministerio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 BIO2011-26741 PATOGENOS DE RNA DE PLANTAS: INTERACCION CON EL HUESPED Y DESARROLLO DE HERRAMIENTAS BIOTECNOLOGICAS |
| dc.rights.none.fl_str_mv |
open access http://purl.org/coar/access_right/c_abf2 Reconocimiento - No comercial (by-nc) http://creativecommons.org/licenses/by-nc/4.0/ |
| dc.rights.openaire.fl_str_mv |
info:eu-repo/semantics/openAccess |
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open access http://purl.org/coar/access_right/c_abf2 Reconocimiento - No comercial (by-nc) http://creativecommons.org/licenses/by-nc/4.0/ |
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openAccess |
| dc.format.none.fl_str_mv |
application/pdf |
| dc.publisher.none.fl_str_mv |
Oxford University Press (OUP): Molecular Biology and Evolution |
| publisher.none.fl_str_mv |
Oxford University Press (OUP): Molecular Biology and Evolution |
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reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia instname:Universitat Politècnica de València (UPV) |
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Universitat Politècnica de València (UPV) |
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RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia |
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RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia |
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1869406889937207296 |
| spelling |
Experimental evolution of pseudogenization and gene loss in a plant RNA virusZwart, Mark PeterWillemsen, AnoukElena Fito, Santiago FcoDaròs, José-Antonio|||0000-0002-6535-2889Genome evolutionPlant virusHorizontal gene transferPseudogenizationFitnessNext-generation sequencing[EN] Viruses have evolved highly streamlined genomes and a variety of mechanisms to compress them, suggesting that genome size is under strong selection. Horizontal gene transfer has, on the other hand, played an important role in virus evolution. However, evolution cannot integrate initially nonfunctional sequences into the viral genome if they are rapidly purged by selection. Here we report on the experimental evolution of pseudogenization in virus genomes using a plant RNA virus expressing a heterologous gene. When long 9-week passages were performed, the added gene was lost in all lineages, whereas viruses with large genomic deletions were fixed in only two out of ten 3-week lineages and none in 1-week lineages. Illumina next-generation sequencing revealed considerable convergent evolution in the 9- and 3-week lineages with genomic deletions. Genome size was correlated to within-host competitive fitness, although there was no correlation with virus accumulation or virulence. Within-host competitive fitness of the 3-week virus lineages without genomic deletions was higher than for the 1-week lineages. Our results show that the strength of selection for a reduced genome size and the rate of pseudogenization depend on demographic conditions. Moreover, for the 3-week passage condition, we observed increases in within-host fitness, whereas selection was not strong enough to quickly remove the nonfunctional heterologous gene. These results suggest a demographically determined "sweet spot" might exist, where heterologous insertions are not immediately lost while evolution can act to integrate them into the viral genome.The authors thank Alejandro Manzano Marin for his bioinformatics guidance with the Illumina analysis and Francisca de la Iglesia, Paula Agudo, and Angels Prosper for technical support. This project was made possible through the support of grant 22371 from the John Templeton Foundation to S. F. E. The opinions expressed in this publication are those of the authors and do not necessarily reflect the views of John Templeton Foundation. Additional support was received from the Spanish Direccion General de Investigacion Cientifica y Tecnica grants BFU2012-30805 to S. F. E, JCI2011-10379 to M.P.Z, and BIO2011-26741 to J.A.D., and by a Rubicon grant from the Netherlands Organization for Scientific Research (www.nwo.nl) to M.P.Z.Oxford University Press (OUP): Molecular Biology and EvolutionInstituto Universitario Mixto de Biología Molecular y Celular de PlantasMinisterio de Ciencia e InnovaciónJohn Templeton FoundationMinisterio de Economía y CompetitividadRepositorio Institucional de la Universitat Politècnica de València Riunet20142014-01-01journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://riunet.upv.es/handle/10251/72658reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valénciainstname:Universitat Politècnica de València (UPV)InglésengJohn Templeton Foundation https://doi.org/10.13039/100000925 22371Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 BFU2012-30805 EVOLUTIONARY SYSTEMS VIROLOGY: EPISTASIS AND THE RUGGEDNESS OF ADAPTIVE LANDSCAPES, MUTATIONS IN REGULATORY SEQUENCES, AND THE HOST DETERMINANTS OF VIRAL FITNESSMinisterio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 JCI-2011-10379 JCI-2011-10379Ministerio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 BIO2011-26741 PATOGENOS DE RNA DE PLANTAS: INTERACCION CON EL HUESPED Y DESARROLLO DE HERRAMIENTAS BIOTECNOLOGICASopen accesshttp://purl.org/coar/access_right/c_abf2Reconocimiento - No comercial (by-nc) http://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:riunet.upv.es:10251/726582026-06-13T07:49:27Z |
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15,198674 |