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...

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Autores: Zwart, Mark Peter, Willemsen, Anouk, Elena Fito, Santiago Fco, Daròs, José-Antonio|||0000-0002-6535-2889
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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repository_id_str
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
rights_invalid_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/
eu_rights_str_mv 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
dc.source.none.fl_str_mv reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
instname:Universitat Politècnica de València (UPV)
instname_str Universitat Politècnica de València (UPV)
reponame_str RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
collection RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
repository.name.fl_str_mv
repository.mail.fl_str_mv
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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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