Dataset Information

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

ABSTRACT: 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.

SUBMITTER: Stitz M

PROVIDER: S-EPMC10183831 | biostudies-literature | 2023 May

REPOSITORIES: biostudies-literature

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

Stitz Michael M Kuster David D Reinert Maximilian M Schepetilnikov Mikhail M Berthet Béatrice B Reyes-Hernández Jazmin J Janocha Denis D Artins Anthony A Boix Marc M Henriques Rossana R Pfeiffer Anne A Lohmann Jan J Gaquerel Emmanuel E Maizel Alexis A

The EMBO journal 20230406 10

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 bran ...[more]

PMID: 37021425

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Project description:Lateral root (LR) formation is a vital organogenetic process that determines the root architecture in plants. The number of root branches governs the degree of anchorage, efficiency of nutrients acquisition, and water uptake. The molecular pathways involved in LR formation have been extensively studied in Arabidopsis thaliana (At). A plant hormone, Auxin, is a key regulator of root development and promotes LR formation in plants. A plethora of Arabidopsis genes have been identified to regulate LR initiation, patterning, and emergence processes. Recently, the involvement of flowering time control pathways and circadian clock pathways in LR development has come to light, but the connecting link between these processes is still missing. We have established that GIGANTEA (GI), a key component of photoperiodic flowering, can regulate the formation of LRs in Arabidopsis. GI is known to be involved in red light signaling and circadian clock signaling pathways. Here, we report that over-expression of GI enhances LR formation in red light in At. Real-time PCR analysis shows that GI positively regulates the transcription of TRANSPORT INHIBITOR RESPONSE 1 (TIR1) which is an upstream component of auxin signaling. Furthermore, gi-100 mutant downregulates the LR initiation signaling gene, AUXIN RESPONSE FACTOR 7 (ARF7), and its downstream target gene, LATERAL ORGAN BOUNDARIES-DOMAIN 16 (LBD16). Hence, GI acts as a positive regulator of IAA14-ARF7-LBD16 modules during LR initiation. We have also checked the effect of GI on the expression of NAC1 and AIR3 genes which are controlled by TIR1 during LR formation. Our results show that GI induces the NAC1 transcription and its downstream gene, AIR3 expression, which leads to the enhancement of LR initiation. Taken together, our results suggest that GI controls the expression of TIR1 to govern auxin signaling during LR formation in presence of red light and GI can act as a link between circadian clock signaling, flowering time control pathways, light signaling, and lateral root development pathways.

Project description:Background and aimsLATERAL ORGAN BOUNDARIES DOMAIN 29 (LBD29), an important molecule downstream of auxin response factors ARF7 and ARF19, has a critical role in lateral root formation in Arabidopsis thaliana. The cell cycle activation of pericycle cells and their speciﬁcation triggered by auxin are crucial for the initiation of lateral roots. In this study, we attempted to determine whether LBD29 is involved in auxin signalling and/or cell cycle regulation and to characterize the roles of LBD29 in these processes.MethodsThe impact of LBD29 on cell cycling progression in pericycle cells was investigated in lbd29 loss-of-function mutant or LBD29-over-expressing plants. The cell cycle was determined by measuring the expression of some cell cycle-related genes using in situ hybridization and quantitative real-time reverse transcription-PCR (qRT-PCR). Furthermore, the cell division in the root explants from either the lbd29 mutant, LBD29-over-expressing plants or the wild type grown in auxin-rich media was also analysed and compared by the distribution of DR5:β-glucuronidase (GUS) in the primordia or by the expression of PIN-FORMED (PIN) members and PLETHROA 1 (PLT1) which represented the auxin response by the pericycle cells.Key resultslbd29 mutation resulted in reduced numbers of lateral roots and primordia, whereas LBD29 over-expression resulted in more lateral root and primordia formation than in the wild type. More importantly, the level of LBD29 expression was found to be positively correlated with the level of expression of cell cycle-related genes and correlated with the numbers of subcellular organelles found in pericycle cells in the maturation zone. In addition, an in vitro experiment using root explants demonstrated that the presence of LBD29 was required for the maintenance of the cell division capacity of the pericycle. Furthermore, LBD29 appeared to modify PIN-dependent auxin signalling in the primordia since there was a correlated association between the expression of PINs, PLT1 and DR5:GUS and the expression of LBD29.ConclusionsThe ability of LBD29 to regulate lateral root initiation is associated with its maintenance of the cell division capacity of the pericycle in response to auxin and its involvement in the auxin signalling pathway.

Dataset Information

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

Publications

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

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