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...
| Autores: | , , , , , , , , , , , , , |
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| Tipo de documento: | artigo |
| Estado: | Versão publicada |
| Data de publicação: | 2023 |
| País: | España |
| Recursos: | Consejo Superior de Investigaciones Científicas (CSIC) |
| Repositório: | DIGITAL.CSIC. Repositorio Institucional del CSIC |
| OAI Identifier: | oai:digital.csic.es:10261/339611 |
| Acesso em linha: | http://hdl.handle.net/10261/339611 https://api.elsevier.com/content/abstract/scopus_id/85151954951 |
| Access Level: | Acceso aberto |
| Palavra-chave: | Arabidopsis thaliana Auxin Lateral root Metabolism TOR |
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oai:digital.csic.es:10261/339611 |
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España |
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TOR acts as a metabolic gatekeeper for auxin-dependent lateral root initiation in Arabidopsis thaliana 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 Arabidopsis thaliana Auxin Lateral root Metabolism TOR 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. 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 reviewed EMBO Press http://hdl.handle.net/10261/339611 https://api.elsevier.com/content/abstract/scopus_id/85151954951 |
| 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 |
| 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 |
| topic |
Arabidopsis thaliana Auxin Lateral root Metabolism TOR |
| topic_facet |
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 |
| format |
article |
| status_str |
publishedVersion |
| url |
http://hdl.handle.net/10261/339611 https://api.elsevier.com/content/abstract/scopus_id/85151954951 |
| eu_rights_str_mv |
openAccess |
| publisher |
EMBO Press |
| institution |
Consejo Superior de Investigaciones Científicas (CSIC) |
| collection |
DIGITAL.CSIC. Repositorio Institucional del CSIC |
| reponame_str |
DIGITAL.CSIC. Repositorio Institucional del CSIC |
| instname_str |
Consejo Superior de Investigaciones Científicas (CSIC) |
| _version_ |
1878437509379129344 |
| publishDateSort |
2023 |
| author_browse |
Artins, Anthony Berthet, Béatrice Boix, Marc Gaquerel, Emmanuel Henriques, Rossana Janocha, Denis Kuster, David Lohmann, Jan U. Maizel, Alexis Pfeiffer, Anne Reinert, Maximilian Reyes-Hernández, Jazmín Schepetilnikov, Mikhail Stitz, Michael |
| publisherStr |
EMBO Press |
| score |
6,9303427 |