TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana

Plant organogenesis requires matching the available metabolic resources to developmental programs. In Arabidopsis, the root system is determined by primary root-derived lateral roots (LRs), and adventitious roots (ARs) formed from non-root organs. Lateral root formation entails the auxin-dependent a...

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Autores: Stitz, Michael, Kuster, David, Reinert, Maximilian, Schepetilnikov, Mikhail, Berthet, Béatrice, Reyes-Hernández, Jazmín, Janocha, Denis, Artins, Anthony, Boix, Marc, Henriques, Rossana, Pfeiffer, Anne, Lohmann, Jan U., Gaquerel, Emmanuel, Maizel, Alexis
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/339611
Acceso en línea:http://hdl.handle.net/10261/339611
https://api.elsevier.com/content/abstract/scopus_id/85151954951
Access Level:acceso abierto
Palabra clave:Arabidopsis thaliana
Auxin
Lateral root
Metabolism
TOR
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spelling TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thalianaStitz, MichaelKuster, DavidReinert, MaximilianSchepetilnikov, MikhailBerthet, BéatriceReyes-Hernández, JazmínJanocha, DenisArtins, AnthonyBoix, MarcHenriques, RossanaPfeiffer, AnneLohmann, Jan U.Gaquerel, EmmanuelMaizel, AlexisArabidopsis thalianaAuxinLateral rootMetabolismTORPlant organogenesis requires matching the available metabolic resources to developmental programs. In Arabidopsis, the root system is determined by primary root-derived lateral roots (LRs), and adventitious roots (ARs) formed from non-root organs. Lateral root formation entails the auxin-dependent activation of transcription factors ARF7, ARF19, and LBD16. Adventitious root formation relies on LBD16 activation by auxin and WOX11. The allocation of shoot-derived sugar to the roots influences branching, but how its availability is sensed for LRs formation remains unknown. We combine metabolic profiling with cell-specific interference to show that LRs switch to glycolysis and consume carbohydrates. The target-of-rapamycin (TOR) kinase is activated in the lateral root domain. Interfering with TOR kinase blocks LR initiation while promoting AR formation. The target-of-rapamycin inhibition marginally affects the auxin-induced transcriptional response of the pericycle but attenuates the translation of ARF19, ARF7, and LBD16. TOR inhibition induces WOX11 transcription in these cells, yet no root branching occurs as TOR controls LBD16 translation. TOR is a central gatekeeper for root branching that integrates local auxin-dependent pathways with systemic metabolic signals, modulating the translation of auxin-induced genes.The authors gratefully acknowledge [...] the Cluster of Excellence Cellular Networks of the University of Heidelberg (CellNetworks) through grant EcTOP6 “Metabolism and Development” and the German Research Foundation (DFG) through grants INST 35/1314-1 FUGG, INST 35/1503-1 FUGG and FOR2581. Open Access funding enabled and organized by ProjektDEAL. Open Access funding enabled and organized by Projekt DEAL.Peer reviewedEMBO PressUniversity of HeidelbergGerman Research FoundationProjekt DEALKuster, David [0000-0002-8157-9223]Schepetilnikov, Mikhail [0000-0002-9043-3592]#NODATA#Reyes-Hernández, Jazmín [0000-0001-9748-9751]Janocha, Denis [0000-0003-1257-9577]Artins, Anthony [0000-0003-0458-259X]Lohmann, Jan U. [0000-0003-3667-187X]Gaquerel, Emmanuel [0000-0003-0796-6417]Maizel, Alexis [0000-0001-6843-1059]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/339611https://api.elsevier.com/content/abstract/scopus_id/85151954951reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésStitz, Michael; Kuster, David; Reinert, Maximilian; Schepetilnikov, Mikhail; Berthet, Béatrice; Reyes-Hernández, Jazmín; Janocha, Denis; Artins, Anthony; Boix, Marc; Henriques, Rossana; Pfeiffer, Anne; Lohmann, Jan U.; Gaquerel, Emmanuel; Maizel, Alexis; 2023; TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana [Dataset]; EMBO Press; https://doi.org/10.15252/embj.2022111273https://doi.org/10.15252/embj.2022111273Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3396112026-05-22T06:33:51Z
dc.title.none.fl_str_mv TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana
title TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana
spellingShingle TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana
Stitz, Michael
Arabidopsis thaliana
Auxin
Lateral root
Metabolism
TOR
title_short TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana
title_full TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana
title_fullStr TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana
title_full_unstemmed TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana
title_sort TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana
dc.creator.none.fl_str_mv Stitz, Michael
Kuster, David
Reinert, Maximilian
Schepetilnikov, Mikhail
Berthet, Béatrice
Reyes-Hernández, Jazmín
Janocha, Denis
Artins, Anthony
Boix, Marc
Henriques, Rossana
Pfeiffer, Anne
Lohmann, Jan U.
Gaquerel, Emmanuel
Maizel, Alexis
author Stitz, Michael
author_facet Stitz, Michael
Kuster, David
Reinert, Maximilian
Schepetilnikov, Mikhail
Berthet, Béatrice
Reyes-Hernández, Jazmín
Janocha, Denis
Artins, Anthony
Boix, Marc
Henriques, Rossana
Pfeiffer, Anne
Lohmann, Jan U.
Gaquerel, Emmanuel
Maizel, Alexis
author_role author
author2 Kuster, David
Reinert, Maximilian
Schepetilnikov, Mikhail
Berthet, Béatrice
Reyes-Hernández, Jazmín
Janocha, Denis
Artins, Anthony
Boix, Marc
Henriques, Rossana
Pfeiffer, Anne
Lohmann, Jan U.
Gaquerel, Emmanuel
Maizel, Alexis
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv University of Heidelberg
German Research Foundation
Projekt DEAL
Kuster, David [0000-0002-8157-9223]
Schepetilnikov, Mikhail [0000-0002-9043-3592]
#NODATA#
Reyes-Hernández, Jazmín [0000-0001-9748-9751]
Janocha, Denis [0000-0003-1257-9577]
Artins, Anthony [0000-0003-0458-259X]
Lohmann, Jan U. [0000-0003-3667-187X]
Gaquerel, Emmanuel [0000-0003-0796-6417]
Maizel, Alexis [0000-0001-6843-1059]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Arabidopsis thaliana
Auxin
Lateral root
Metabolism
TOR
topic Arabidopsis thaliana
Auxin
Lateral root
Metabolism
TOR
description Plant organogenesis requires matching the available metabolic resources to developmental programs. In Arabidopsis, the root system is determined by primary root-derived lateral roots (LRs), and adventitious roots (ARs) formed from non-root organs. Lateral root formation entails the auxin-dependent activation of transcription factors ARF7, ARF19, and LBD16. Adventitious root formation relies on LBD16 activation by auxin and WOX11. The allocation of shoot-derived sugar to the roots influences branching, but how its availability is sensed for LRs formation remains unknown. We combine metabolic profiling with cell-specific interference to show that LRs switch to glycolysis and consume carbohydrates. The target-of-rapamycin (TOR) kinase is activated in the lateral root domain. Interfering with TOR kinase blocks LR initiation while promoting AR formation. The target-of-rapamycin inhibition marginally affects the auxin-induced transcriptional response of the pericycle but attenuates the translation of ARF19, ARF7, and LBD16. TOR inhibition induces WOX11 transcription in these cells, yet no root branching occurs as TOR controls LBD16 translation. TOR is a central gatekeeper for root branching that integrates local auxin-dependent pathways with systemic metabolic signals, modulating the translation of auxin-induced genes.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
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/10261/339611
https://api.elsevier.com/content/abstract/scopus_id/85151954951
url http://hdl.handle.net/10261/339611
https://api.elsevier.com/content/abstract/scopus_id/85151954951
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Stitz, Michael; Kuster, David; Reinert, Maximilian; Schepetilnikov, Mikhail; Berthet, Béatrice; Reyes-Hernández, Jazmín; Janocha, Denis; Artins, Anthony; Boix, Marc; Henriques, Rossana; Pfeiffer, Anne; Lohmann, Jan U.; Gaquerel, Emmanuel; Maizel, Alexis; 2023; TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana [Dataset]; EMBO Press; https://doi.org/10.15252/embj.2022111273
https://doi.org/10.15252/embj.2022111273
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv EMBO Press
publisher.none.fl_str_mv EMBO 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
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.811543

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