Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs

Autores
Traubenik, Laura Soledad; Reynoso, Mauricio Alberto; Hobecker, Karen Vanesa; Lancia, Marcos; Hummel, Maureen; Rosen, Benjamin D.; Town, Christopher D.; Bailey Serres, Julia; Blanco, Flavio Antonio; Zanetti, María Eugenia
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Translational control is a widespread mechanism that allows the cell to rapidly modulate gene expression in order to provide flexibility and adaptability to eukaryotic organisms. We applied translating ribosome affinity purification combined with RNA sequencing to characterize translational regulation of mRNAs at early stages of the nitrogen-fixing symbiosis established between Medicago truncatula and Sinorhizobium meliloti. Our analysis revealed a poor correlation between transcriptional and translational changes and identified hundreds of regulated protein-coding and long noncoding RNAs (lncRNAs), some of which are regulated in specific cell types. We demonstrated that a short variant of the lncRNA Trans-acting small interference RNA3 (TAS3) increased its association to the translational machinery in response to rhizobia. Functional analysis revealed that this short variant of TAS3 might act as a target mimic that captures microRNA390, contributing to reduce trans acting small interference Auxin Response Factor production and modulating nodule formation and rhizobial infection. The analysis of alternative transcript variants identified a translationally upregulated mRNA encoding subunit 3 of the SUPERKILLER complex (SKI3), which participates in mRNA decay. Knockdown of SKI3 decreased nodule initiation and development, as well as the survival of bacteria within nodules. Our results highlight the importance of translational control and mRNA decay pathways for the successful establishment of the nitrogen-fixing symbiosis.
Facultad de Ciencias Exactas
Instituto de Biotecnologia y Biologia Molecular
Materia
Ciencias Exactas
Biología
Cell biology
Root Cells
Nitrogen-Fixing Symbiosis
Coding and Noncoding RNAs
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by-nc-sa/4.0/
Repositorio
SEDICI (UNLP)
Institución
Universidad Nacional de La Plata
OAI Identificador
oai:sedici.unlp.edu.ar:10915/124792
Acceder
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oai_identifier_str oai:sedici.unlp.edu.ar:10915/124792
network_acronym_str SEDICI
repository_id_str 1329
network_name_str SEDICI (UNLP)
spelling Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAsTraubenik, Laura SoledadReynoso, Mauricio AlbertoHobecker, Karen VanesaLancia, MarcosHummel, MaureenRosen, Benjamin D.Town, Christopher D.Bailey Serres, JuliaBlanco, Flavio AntonioZanetti, María EugeniaCiencias ExactasBiologíaCell biologyRoot CellsNitrogen-Fixing SymbiosisCoding and Noncoding RNAsTranslational control is a widespread mechanism that allows the cell to rapidly modulate gene expression in order to provide flexibility and adaptability to eukaryotic organisms. We applied translating ribosome affinity purification combined with RNA sequencing to characterize translational regulation of mRNAs at early stages of the nitrogen-fixing symbiosis established between <i>Medicago truncatula</i> and <i>Sinorhizobium meliloti</i>. Our analysis revealed a poor correlation between transcriptional and translational changes and identified hundreds of regulated protein-coding and long noncoding RNAs (lncRNAs), some of which are regulated in specific cell types. We demonstrated that a short variant of the lncRNA <i>Trans-acting small interference RNA3</i> (<i>TAS3</i>) increased its association to the translational machinery in response to rhizobia. Functional analysis revealed that this short variant of <i>TAS3</i> might act as a target mimic that captures microRNA390, contributing to reduce trans acting small interference Auxin Response Factor production and modulating nodule formation and rhizobial infection. The analysis of alternative transcript variants identified a translationally upregulated mRNA encoding subunit 3 of the SUPERKILLER complex (SKI3), which participates in mRNA decay. Knockdown of <i>SKI3</i> decreased nodule initiation and development, as well as the survival of bacteria within nodules. Our results highlight the importance of translational control and mRNA decay pathways for the successful establishment of the nitrogen-fixing symbiosis.Facultad de Ciencias ExactasInstituto de Biotecnologia y Biologia Molecular2020-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionArticulohttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdf352-373http://sedici.unlp.edu.ar/handle/10915/124792enginfo:eu-repo/semantics/altIdentifier/issn/1532-298Xinfo:eu-repo/semantics/altIdentifier/issn/1040-4651info:eu-repo/semantics/altIdentifier/pmid/33590195info:eu-repo/semantics/altIdentifier/pmid/31748328info:eu-repo/semantics/altIdentifier/doi/10.1105/tpc.19.00647info:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-sa/4.0/Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)reponame:SEDICI (UNLP)instname:Universidad Nacional de La Platainstacron:UNLP2025-10-15T11:21:41Zoai:sedici.unlp.edu.ar:10915/124792Institucionalhttp://sedici.unlp.edu.ar/Universidad públicaNo correspondehttp://sedici.unlp.edu.ar/oai/snrdalira@sedici.unlp.edu.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:13292025-10-15 11:21:41.909SEDICI (UNLP) - Universidad Nacional de La Platafalse
dc.title.none.fl_str_mv Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs
title Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs
spellingShingle Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs
Traubenik, Laura Soledad
Ciencias Exactas
Biología
Cell biology
Root Cells
Nitrogen-Fixing Symbiosis
Coding and Noncoding RNAs
title_short Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs
title_full Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs
title_fullStr Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs
title_full_unstemmed Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs
title_sort Reprogramming of Root Cells during Nitrogen-Fixing Symbiosis Involves Dynamic Polysome Association of Coding and Noncoding RNAs
dc.creator.none.fl_str_mv Traubenik, Laura Soledad
Reynoso, Mauricio Alberto
Hobecker, Karen Vanesa
Lancia, Marcos
Hummel, Maureen
Rosen, Benjamin D.
Town, Christopher D.
Bailey Serres, Julia
Blanco, Flavio Antonio
Zanetti, María Eugenia
author Traubenik, Laura Soledad
author_facet Traubenik, Laura Soledad
Reynoso, Mauricio Alberto
Hobecker, Karen Vanesa
Lancia, Marcos
Hummel, Maureen
Rosen, Benjamin D.
Town, Christopher D.
Bailey Serres, Julia
Blanco, Flavio Antonio
Zanetti, María Eugenia
author_role author
author2 Reynoso, Mauricio Alberto
Hobecker, Karen Vanesa
Lancia, Marcos
Hummel, Maureen
Rosen, Benjamin D.
Town, Christopher D.
Bailey Serres, Julia
Blanco, Flavio Antonio
Zanetti, María Eugenia
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Ciencias Exactas
Biología
Cell biology
Root Cells
Nitrogen-Fixing Symbiosis
Coding and Noncoding RNAs
topic Ciencias Exactas
Biología
Cell biology
Root Cells
Nitrogen-Fixing Symbiosis
Coding and Noncoding RNAs
dc.description.none.fl_txt_mv Translational control is a widespread mechanism that allows the cell to rapidly modulate gene expression in order to provide flexibility and adaptability to eukaryotic organisms. We applied translating ribosome affinity purification combined with RNA sequencing to characterize translational regulation of mRNAs at early stages of the nitrogen-fixing symbiosis established between <i>Medicago truncatula</i> and <i>Sinorhizobium meliloti</i>. Our analysis revealed a poor correlation between transcriptional and translational changes and identified hundreds of regulated protein-coding and long noncoding RNAs (lncRNAs), some of which are regulated in specific cell types. We demonstrated that a short variant of the lncRNA <i>Trans-acting small interference RNA3</i> (<i>TAS3</i>) increased its association to the translational machinery in response to rhizobia. Functional analysis revealed that this short variant of <i>TAS3</i> might act as a target mimic that captures microRNA390, contributing to reduce trans acting small interference Auxin Response Factor production and modulating nodule formation and rhizobial infection. The analysis of alternative transcript variants identified a translationally upregulated mRNA encoding subunit 3 of the SUPERKILLER complex (SKI3), which participates in mRNA decay. Knockdown of <i>SKI3</i> decreased nodule initiation and development, as well as the survival of bacteria within nodules. Our results highlight the importance of translational control and mRNA decay pathways for the successful establishment of the nitrogen-fixing symbiosis.
Facultad de Ciencias Exactas
Instituto de Biotecnologia y Biologia Molecular
description Translational control is a widespread mechanism that allows the cell to rapidly modulate gene expression in order to provide flexibility and adaptability to eukaryotic organisms. We applied translating ribosome affinity purification combined with RNA sequencing to characterize translational regulation of mRNAs at early stages of the nitrogen-fixing symbiosis established between <i>Medicago truncatula</i> and <i>Sinorhizobium meliloti</i>. Our analysis revealed a poor correlation between transcriptional and translational changes and identified hundreds of regulated protein-coding and long noncoding RNAs (lncRNAs), some of which are regulated in specific cell types. We demonstrated that a short variant of the lncRNA <i>Trans-acting small interference RNA3</i> (<i>TAS3</i>) increased its association to the translational machinery in response to rhizobia. Functional analysis revealed that this short variant of <i>TAS3</i> might act as a target mimic that captures microRNA390, contributing to reduce trans acting small interference Auxin Response Factor production and modulating nodule formation and rhizobial infection. The analysis of alternative transcript variants identified a translationally upregulated mRNA encoding subunit 3 of the SUPERKILLER complex (SKI3), which participates in mRNA decay. Knockdown of <i>SKI3</i> decreased nodule initiation and development, as well as the survival of bacteria within nodules. Our results highlight the importance of translational control and mRNA decay pathways for the successful establishment of the nitrogen-fixing symbiosis.
publishDate 2020
dc.date.none.fl_str_mv 2020-02
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
Articulo
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://sedici.unlp.edu.ar/handle/10915/124792
url http://sedici.unlp.edu.ar/handle/10915/124792
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/issn/1532-298X
info:eu-repo/semantics/altIdentifier/issn/1040-4651
info:eu-repo/semantics/altIdentifier/pmid/33590195
info:eu-repo/semantics/altIdentifier/pmid/31748328
info:eu-repo/semantics/altIdentifier/doi/10.1105/tpc.19.00647
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
dc.format.none.fl_str_mv application/pdf
352-373
dc.source.none.fl_str_mv reponame:SEDICI (UNLP)
instname:Universidad Nacional de La Plata
instacron:UNLP
reponame_str SEDICI (UNLP)
collection SEDICI (UNLP)
instname_str Universidad Nacional de La Plata
instacron_str UNLP
institution UNLP
repository.name.fl_str_mv SEDICI (UNLP) - Universidad Nacional de La Plata
repository.mail.fl_str_mv alira@sedici.unlp.edu.ar
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score 13.22299

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