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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 principales: Stitz, Michael, Kuster, David, Reinert, Maximilian, Schepetilnikov, Mikhail, Berthet, Béatrice, Reyes‐Hernández, Jazmin, Janocha, Denis, Artins, Anthony, Boix, Marc, Henriques, Rossana, Pfeiffer, Anne, Lohmann, Jan, Gaquerel, Emmanuel, Maizel, Alexis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10183831/
https://www.ncbi.nlm.nih.gov/pubmed/37021425
http://dx.doi.org/10.15252/embj.2022111273
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author Stitz, Michael
Kuster, David
Reinert, Maximilian
Schepetilnikov, Mikhail
Berthet, Béatrice
Reyes‐Hernández, Jazmin
Janocha, Denis
Artins, Anthony
Boix, Marc
Henriques, Rossana
Pfeiffer, Anne
Lohmann, Jan
Gaquerel, Emmanuel
Maizel, Alexis
author_facet Stitz, Michael
Kuster, David
Reinert, Maximilian
Schepetilnikov, Mikhail
Berthet, Béatrice
Reyes‐Hernández, Jazmin
Janocha, Denis
Artins, Anthony
Boix, Marc
Henriques, Rossana
Pfeiffer, Anne
Lohmann, Jan
Gaquerel, Emmanuel
Maizel, Alexis
author_sort Stitz, Michael
collection PubMed
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.
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spelling pubmed-101838312023-05-16 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, Jazmin Janocha, Denis Artins, Anthony Boix, Marc Henriques, Rossana Pfeiffer, Anne Lohmann, Jan Gaquerel, Emmanuel Maizel, Alexis EMBO J Articles 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. John Wiley and Sons Inc. 2023-04-06 /pmc/articles/PMC10183831/ /pubmed/37021425 http://dx.doi.org/10.15252/embj.2022111273 Text en © 2023 The Authors. Published under the terms of the CC BY NC ND 4.0 license https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Articles
Stitz, Michael
Kuster, David
Reinert, Maximilian
Schepetilnikov, Mikhail
Berthet, Béatrice
Reyes‐Hernández, Jazmin
Janocha, Denis
Artins, Anthony
Boix, Marc
Henriques, Rossana
Pfeiffer, Anne
Lohmann, Jan
Gaquerel, Emmanuel
Maizel, Alexis
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
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_short 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
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10183831/
https://www.ncbi.nlm.nih.gov/pubmed/37021425
http://dx.doi.org/10.15252/embj.2022111273
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