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

• Published in: The EMBO journal Vol. 42; no. 10; pp. e111273 - n/a
• Main Authors: 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
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 15.05.2023; EMBO Press; John Wiley and Sons Inc
• Subjects: Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; auxin; Auxins; Availability; Branching; Carbohydrates; Cell differentiation; Cellular Biology; Differentiation (biology); Gene Expression Regulation, Plant; Glycolysis; Indoleacetic Acids - metabolism; Kinases; lateral root; Life Sciences; Metabolism; Organogenesis; Phosphatidylinositol 3-Kinases - genetics; Plant Roots - metabolism; Rapamycin; Roots; Shoots; Sugar; TOR; Transcription activation; Transcription factors; Transcription Factors - metabolism; Translation; Arabidopsis thaliana; metabolism; auxin; lateral root; TOR
• ISSN: 0261-4189; 1460-2075
• DOI: 10.15252/embj.2022111273

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. Synopsis Shoot‐derived sugar promotes lateral root formation, but the mechanism through which it influences cell differentiation in this context is not well understood. Here, we learn that TOR kinase mediates lateral root formation by inducing the translation of lateral root‐promoting transcription factor transcripts in a sugar‐dependent manner. Lateral root formation is an important consumer of shoot‐derived carbon. Pericycle activation requires shoot‐derived carbohydrates and TOR. TOR promotes the translation of transcription factors ARF19, ARF7, and LBD16. TOR suppresses non‐canonical primary root branching by inhibiting WOX11 expression. Shoot‐derived sugar activates TOR signalling to initiate lateral root formation.