Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus

Predicting viral emergence is difficult due to the stochastic nature of the underlying processes and the many factors that govern pathogen evolution. Environmental factors affecting the host, the pathogen and the interaction between both are key in emergence. In particular, infectious disease dynami...

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Detalhes bibliográficos
Autores: González, Rubén, Butkovic, Anamarija, Elena, Santiago F.
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/220719
Acesso em linha:http://hdl.handle.net/10261/220719
Access Level:acceso abierto
Palavra-chave:Evolution of virulence
Experimental evolution
Infection matrix
Host population structure
Potyvirus
Resistance to infection
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spelling Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virusGonzález, RubénButkovic, AnamarijaElena, Santiago F.Evolution of virulenceExperimental evolutionInfection matrixHost population structurePotyvirusResistance to infectionPredicting viral emergence is difficult due to the stochastic nature of the underlying processes and the many factors that govern pathogen evolution. Environmental factors affecting the host, the pathogen and the interaction between both are key in emergence. In particular, infectious disease dynamics are affected by spatiotemporal heterogeneity in their environments. A broad knowledge of these factors will allow better estimating where and when viral emergence is more likely to occur. Here, we investigate how the population structure for susceptibility-to-infection genes of the plant Arabidopsis thaliana shapes the evolution of Turnip mosaic virus (TuMV). For doing so we have evolved TuMV lineages in two radically different host population structures: (1) a metapopulation subdivided into six demes (subpopulations); each one being composed of individuals from only one of six possible A. thaliana ecotypes and (2) a well-mixed population constituted by equal number of plants from the same six A. thaliana ecotypes. These two populations were evolved for twelve serial passages. At the end of the experimental evolution, we found faster adaptation of TuMV to each ecotype in the metapopulation than in the well-mixed heterogeneous host populations. However, viruses evolved in well-mixed populations were more pathogenic and infectious than viruses evolved in the metapopulation. Furthermore, the viruses evolved in the demes showed stronger signatures of local specialization than viruses evolved in the well-mixed populations. These results illustrate how the genetic diversity of hosts in an experimental ecosystem favors the evolution of virulence of a pathogen.Work was supported by Spain’s Agencia Estatal de Investigación—FEDER grant BFU2015-65037-P and Generalitat Valenciana grant GRISOLIA/2018/005 to S.F.E. R.G. was supported by Spain’s Agencia Estatal de Investigación pre-doctoral contract BES-2016-077078.Peer reviewedOxford University PressMinisterio de Economía y Competitividad (España)Generalitat ValencianaAgencia Estatal de Investigación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202020202019info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/220719reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BFU2015-65037-Phttps://doi.org/10.1093/ve/vez024Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2207192026-05-22T06:33:51Z
dc.title.none.fl_str_mv Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus
title Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus
spellingShingle Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus
González, Rubén
Evolution of virulence
Experimental evolution
Infection matrix
Host population structure
Potyvirus
Resistance to infection
title_short Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus
title_full Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus
title_fullStr Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus
title_full_unstemmed Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus
title_sort Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus
dc.creator.none.fl_str_mv González, Rubén
Butkovic, Anamarija
Elena, Santiago F.
author González, Rubén
author_facet González, Rubén
Butkovic, Anamarija
Elena, Santiago F.
author_role author
author2 Butkovic, Anamarija
Elena, Santiago F.
author2_role author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
Generalitat Valenciana
Agencia Estatal de Investigación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Evolution of virulence
Experimental evolution
Infection matrix
Host population structure
Potyvirus
Resistance to infection
topic Evolution of virulence
Experimental evolution
Infection matrix
Host population structure
Potyvirus
Resistance to infection
description Predicting viral emergence is difficult due to the stochastic nature of the underlying processes and the many factors that govern pathogen evolution. Environmental factors affecting the host, the pathogen and the interaction between both are key in emergence. In particular, infectious disease dynamics are affected by spatiotemporal heterogeneity in their environments. A broad knowledge of these factors will allow better estimating where and when viral emergence is more likely to occur. Here, we investigate how the population structure for susceptibility-to-infection genes of the plant Arabidopsis thaliana shapes the evolution of Turnip mosaic virus (TuMV). For doing so we have evolved TuMV lineages in two radically different host population structures: (1) a metapopulation subdivided into six demes (subpopulations); each one being composed of individuals from only one of six possible A. thaliana ecotypes and (2) a well-mixed population constituted by equal number of plants from the same six A. thaliana ecotypes. These two populations were evolved for twelve serial passages. At the end of the experimental evolution, we found faster adaptation of TuMV to each ecotype in the metapopulation than in the well-mixed heterogeneous host populations. However, viruses evolved in well-mixed populations were more pathogenic and infectious than viruses evolved in the metapopulation. Furthermore, the viruses evolved in the demes showed stronger signatures of local specialization than viruses evolved in the well-mixed populations. These results illustrate how the genetic diversity of hosts in an experimental ecosystem favors the evolution of virulence of a pathogen.
publishDate 2019
dc.date.none.fl_str_mv 2019
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/220719
url http://hdl.handle.net/10261/220719
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BFU2015-65037-P
https://doi.org/10.1093/ve/vez024

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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