Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking

Autores
Peña, Eduardo José; Ferriol, Inmaculada; Sambade, Adrian; Buschman, Henrick; Niehl, Annette; Elena, Santiago; Rubio, Luis; Heinlein, Manfred
Año de publicación
2014
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The cytoskeleton is a dynamic network composed of filamentous polymers and regulatory proteins that provide a flexible structural scaffold to the cell and plays a fundamental role in developmental processes. Mutations that alter the spatial orientation of the cortical microtubule (MT) array of plants are known to cause important changes in the pattern of cell wall synthesis and developmental phenotypes; however, the consequences of such alterations on other MT-network-associated functions in the cytoplasm are not known. In vivo observations suggested a role of cortical MTs in the formation and movement of Tobacco mosaic virus (TMV) RNA complexes along the endoplasmic reticulum (ER). Thus, to probe the significance of dynamic MT behavior in the coordination of MT-network-associated functions related to TMV infection and, thus, in the formation and transport of RNA complexes in the cytoplasm, we performed an evolution experiment with TMV in Arabidopsis thaliana tor1/spr2 and tor2 mutants with specific defects in MT dynamics and asked whether TMV is sensitive to these changes. We show that the altered cytoskeleton induced genetic changes in TMV that were correlated with efficient spread of infection in the mutant hosts. These observations demonstrate a role of dynamic MT rearrangements and of the MT-associated protein TORTIFOLIA1/SPIRAL2 in cellular functions related to virus spread and indicate that MT dynamics and MT-associated proteins represent constraints for virus evolution and adaptation. The results highlight the importance of the dynamic plasticity of the MT network in directing cytoplasmic functions in macromolecular assembly and trafficking and illustrate the value of experimental virus evolution for addressing the cellular functions of dynamic, long-range order systems in multicellular organisms.
Fil: Peña, Eduardo José. Centre National de la Recherche Scientifique. Institut de Biologie Moléculaire des Plantes; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ferriol, Inmaculada. Instituto Valenciano de Investigaciones Agrarias; España
Fil: Sambade, Adrian. Universidad de Valencia; España
Fil: Buschman, Henrick. University of Osnabruck; Alemania
Fil: Niehl, Annette. Universidad de Basilea; Suiza
Fil: Elena, Santiago. Consejo Superior de Investigaciones Científicas; España. Santa Fe Institute; Estados Unidos. Instituto de Biologia Molecular y Celular de Plantas; España
Fil: Rubio, Luis. Instituto Valenciano de Investigaciones Agrarias; España
Fil: Heinlein, Manfred. Centre National de la Recherche Scientifique. Institut de Biologie Moléculaire des Plantes; Francia. Universidad de Basilea; Suiza
Materia
TMV
ARABIDOPSIS
MICROTUBULES
EXPERIMENTAL EVOLUTION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/99904
Acceder
id CONICETDig_409cefe43aad474ad975ae918c1892b0
oai_identifier_str oai:ri.conicet.gov.ar:11336/99904
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA traffickingPeña, Eduardo JoséFerriol, InmaculadaSambade, AdrianBuschman, HenrickNiehl, AnnetteElena, SantiagoRubio, LuisHeinlein, ManfredTMVARABIDOPSISMICROTUBULESEXPERIMENTAL EVOLUTIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The cytoskeleton is a dynamic network composed of filamentous polymers and regulatory proteins that provide a flexible structural scaffold to the cell and plays a fundamental role in developmental processes. Mutations that alter the spatial orientation of the cortical microtubule (MT) array of plants are known to cause important changes in the pattern of cell wall synthesis and developmental phenotypes; however, the consequences of such alterations on other MT-network-associated functions in the cytoplasm are not known. In vivo observations suggested a role of cortical MTs in the formation and movement of Tobacco mosaic virus (TMV) RNA complexes along the endoplasmic reticulum (ER). Thus, to probe the significance of dynamic MT behavior in the coordination of MT-network-associated functions related to TMV infection and, thus, in the formation and transport of RNA complexes in the cytoplasm, we performed an evolution experiment with TMV in Arabidopsis thaliana tor1/spr2 and tor2 mutants with specific defects in MT dynamics and asked whether TMV is sensitive to these changes. We show that the altered cytoskeleton induced genetic changes in TMV that were correlated with efficient spread of infection in the mutant hosts. These observations demonstrate a role of dynamic MT rearrangements and of the MT-associated protein TORTIFOLIA1/SPIRAL2 in cellular functions related to virus spread and indicate that MT dynamics and MT-associated proteins represent constraints for virus evolution and adaptation. The results highlight the importance of the dynamic plasticity of the MT network in directing cytoplasmic functions in macromolecular assembly and trafficking and illustrate the value of experimental virus evolution for addressing the cellular functions of dynamic, long-range order systems in multicellular organisms.Fil: Peña, Eduardo José. Centre National de la Recherche Scientifique. Institut de Biologie Moléculaire des Plantes; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Ferriol, Inmaculada. Instituto Valenciano de Investigaciones Agrarias; EspañaFil: Sambade, Adrian. Universidad de Valencia; EspañaFil: Buschman, Henrick. University of Osnabruck; AlemaniaFil: Niehl, Annette. Universidad de Basilea; SuizaFil: Elena, Santiago. Consejo Superior de Investigaciones Científicas; España. Santa Fe Institute; Estados Unidos. Instituto de Biologia Molecular y Celular de Plantas; EspañaFil: Rubio, Luis. Instituto Valenciano de Investigaciones Agrarias; EspañaFil: Heinlein, Manfred. Centre National de la Recherche Scientifique. Institut de Biologie Moléculaire des Plantes; Francia. Universidad de Basilea; SuizaPublic Library of Science2014-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/99904Peña, Eduardo José; Ferriol, Inmaculada; Sambade, Adrian; Buschman, Henrick; Niehl, Annette; et al.; Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking; Public Library of Science; Plos One; 9; 8; 8-2014; 1-71932-6203CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0105364info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0105364info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:46:00Zoai:ri.conicet.gov.ar:11336/99904instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:46:00.579CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking
title Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking
spellingShingle Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking
Peña, Eduardo José
TMV
ARABIDOPSIS
MICROTUBULES
EXPERIMENTAL EVOLUTION
title_short Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking
title_full Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking
title_fullStr Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking
title_full_unstemmed Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking
title_sort Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking
dc.creator.none.fl_str_mv Peña, Eduardo José
Ferriol, Inmaculada
Sambade, Adrian
Buschman, Henrick
Niehl, Annette
Elena, Santiago
Rubio, Luis
Heinlein, Manfred
author Peña, Eduardo José
author_facet Peña, Eduardo José
Ferriol, Inmaculada
Sambade, Adrian
Buschman, Henrick
Niehl, Annette
Elena, Santiago
Rubio, Luis
Heinlein, Manfred
author_role author
author2 Ferriol, Inmaculada
Sambade, Adrian
Buschman, Henrick
Niehl, Annette
Elena, Santiago
Rubio, Luis
Heinlein, Manfred
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv TMV
ARABIDOPSIS
MICROTUBULES
EXPERIMENTAL EVOLUTION
topic TMV
ARABIDOPSIS
MICROTUBULES
EXPERIMENTAL EVOLUTION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The cytoskeleton is a dynamic network composed of filamentous polymers and regulatory proteins that provide a flexible structural scaffold to the cell and plays a fundamental role in developmental processes. Mutations that alter the spatial orientation of the cortical microtubule (MT) array of plants are known to cause important changes in the pattern of cell wall synthesis and developmental phenotypes; however, the consequences of such alterations on other MT-network-associated functions in the cytoplasm are not known. In vivo observations suggested a role of cortical MTs in the formation and movement of Tobacco mosaic virus (TMV) RNA complexes along the endoplasmic reticulum (ER). Thus, to probe the significance of dynamic MT behavior in the coordination of MT-network-associated functions related to TMV infection and, thus, in the formation and transport of RNA complexes in the cytoplasm, we performed an evolution experiment with TMV in Arabidopsis thaliana tor1/spr2 and tor2 mutants with specific defects in MT dynamics and asked whether TMV is sensitive to these changes. We show that the altered cytoskeleton induced genetic changes in TMV that were correlated with efficient spread of infection in the mutant hosts. These observations demonstrate a role of dynamic MT rearrangements and of the MT-associated protein TORTIFOLIA1/SPIRAL2 in cellular functions related to virus spread and indicate that MT dynamics and MT-associated proteins represent constraints for virus evolution and adaptation. The results highlight the importance of the dynamic plasticity of the MT network in directing cytoplasmic functions in macromolecular assembly and trafficking and illustrate the value of experimental virus evolution for addressing the cellular functions of dynamic, long-range order systems in multicellular organisms.
Fil: Peña, Eduardo José. Centre National de la Recherche Scientifique. Institut de Biologie Moléculaire des Plantes; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ferriol, Inmaculada. Instituto Valenciano de Investigaciones Agrarias; España
Fil: Sambade, Adrian. Universidad de Valencia; España
Fil: Buschman, Henrick. University of Osnabruck; Alemania
Fil: Niehl, Annette. Universidad de Basilea; Suiza
Fil: Elena, Santiago. Consejo Superior de Investigaciones Científicas; España. Santa Fe Institute; Estados Unidos. Instituto de Biologia Molecular y Celular de Plantas; España
Fil: Rubio, Luis. Instituto Valenciano de Investigaciones Agrarias; España
Fil: Heinlein, Manfred. Centre National de la Recherche Scientifique. Institut de Biologie Moléculaire des Plantes; Francia. Universidad de Basilea; Suiza
description The cytoskeleton is a dynamic network composed of filamentous polymers and regulatory proteins that provide a flexible structural scaffold to the cell and plays a fundamental role in developmental processes. Mutations that alter the spatial orientation of the cortical microtubule (MT) array of plants are known to cause important changes in the pattern of cell wall synthesis and developmental phenotypes; however, the consequences of such alterations on other MT-network-associated functions in the cytoplasm are not known. In vivo observations suggested a role of cortical MTs in the formation and movement of Tobacco mosaic virus (TMV) RNA complexes along the endoplasmic reticulum (ER). Thus, to probe the significance of dynamic MT behavior in the coordination of MT-network-associated functions related to TMV infection and, thus, in the formation and transport of RNA complexes in the cytoplasm, we performed an evolution experiment with TMV in Arabidopsis thaliana tor1/spr2 and tor2 mutants with specific defects in MT dynamics and asked whether TMV is sensitive to these changes. We show that the altered cytoskeleton induced genetic changes in TMV that were correlated with efficient spread of infection in the mutant hosts. These observations demonstrate a role of dynamic MT rearrangements and of the MT-associated protein TORTIFOLIA1/SPIRAL2 in cellular functions related to virus spread and indicate that MT dynamics and MT-associated proteins represent constraints for virus evolution and adaptation. The results highlight the importance of the dynamic plasticity of the MT network in directing cytoplasmic functions in macromolecular assembly and trafficking and illustrate the value of experimental virus evolution for addressing the cellular functions of dynamic, long-range order systems in multicellular organisms.
publishDate 2014
dc.date.none.fl_str_mv 2014-08
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/99904
Peña, Eduardo José; Ferriol, Inmaculada; Sambade, Adrian; Buschman, Henrick; Niehl, Annette; et al.; Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking; Public Library of Science; Plos One; 9; 8; 8-2014; 1-7
1932-6203
CONICET Digital
CONICET
url http://hdl.handle.net/11336/99904
identifier_str_mv Peña, Eduardo José; Ferriol, Inmaculada; Sambade, Adrian; Buschman, Henrick; Niehl, Annette; et al.; Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking; Public Library of Science; Plos One; 9; 8; 8-2014; 1-7
1932-6203
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0105364
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0105364
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1844613437619961856
score 13.070432

Publicaciones similares