Mutations in the Arabidopsis ROL17/isopropylmalate synthase 1 locus alter amino acid content, modify the TOR network, and suppress the root hair cell development mutant lrx1

Schaufelberger, Myriam; Galbier, Florian; Herger, Aline; Francisco, Rita de Brito; Roffler, Stefan; Clément, Gilles; Diet, Anouck; Hörtensteiner, Stefan; Wicker, Thomas; Ringli, Christoph

doi:10.1093/jxb/ery463

Cited by 36 publications

(45 citation statements)

References 76 publications

(132 reference statements)

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“…IPMS1 is the first committed step of leucine biosynthesis; accordingly, ipms1 mutants exhibit broad defects in free amino acid accumulation ( Cao et al, 2019 ). While the exact cause remains undefined, the disruption of amino acid metabolism in ipms1 mutants apparently increases cellular TOR activity ( Cao et al, 2019 ; Schaufelberger et al, 2019 ). Reducing TOR activity by treating ipms1 mutants with ATP-competitive TOR inhibitors rescues the ipms1 actin organization phenotype, which suggests that TOR regulates actin filamentation in plants.…”

Section: Resultsmentioning

confidence: 99%

Parallel global profiling of plant TOR dynamics reveals a conserved role for LARP1 in translation

Scarpin

Leiboff

Brunkard

2020

eLife

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TARGET OF RAPAMYCIN (TOR) is a protein kinase that coordinates eukaryotic metabolism. In mammals, TOR specifically promotes translation of ribosomal protein mRNAs when amino acids are available to support protein synthesis. The mechanisms controlling translation downstream from TOR remain contested, however, and are largely unexplored in plants. To define these mechanisms in plants, we globally profiled the plant TOR-regulated transcriptome, translatome, proteome, and phosphoproteome. We found that TOR regulates ribosome biogenesis in plants at multiple levels, but through mechanisms that do not directly depend on 5′ oligopyrimidine tract motifs (5′TOPs) found in mammalian ribosomal protein mRNAs. We then show that the TOR-LARP1-5′TOP signaling axis is conserved in plants and regulates expression of a core set of eukaryotic 5′TOP mRNAs, as well as new, plant-specific 5′TOP mRNAs. Our study illuminates ancestral roles of the TOR-LARP1-5′TOP metabolic regulatory network and provides evolutionary context for ongoing debates about the molecular function of LARP1.

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Section: Resultsmentioning

confidence: 99%

Parallel global profiling of plant TOR dynamics reveals a conserved role for LARP1 in translation

Scarpin

Leiboff

Brunkard

2020

eLife

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“…DGR2 interferes with ABA-ROP10 signaling and root morphogenesis. CAP1 controls Ca + gradients for RH tip growth (Weiste et al, 2017;Schoenaers et al, 2018;Schaufelberger et al, 2019;Van Leene et al, 2019;Li et al, 2020;Zhu et al, 2020). All these signaling components downstream of TOR and SnRK signaling may control RH growth under Hpx and HpxAs.…”

Section: Energy Constraints and Stress Acclimationmentioning

confidence: 99%

Remodeling of Root Growth Under Combined Arsenic and Hypoxia Stress Is Linked to Nutrient Deprivation

et al. 2020

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Root architecture responds to environmental stress. Stress-induced metabolic and nutritional changes affect the endogenous root development program. Transcriptional and translational changes realize the switch between stem cell proliferation and cell differentiation, lateral root or root hair formation and root functionality for stress acclimation. The current work explores the effects of stress combination of arsenic toxicity (As) and hypoxia (Hpx) on root development in Arabidopsis thaliana. As revealed previously, combined As and Hpx treatment leads to severe nutritional disorder evident from deregulation of root transcriptome and plant mineral contents. Both As and Hpx were identified to pose stress-specific constraints on root development that lead to unique root growth phenotype under their combination. Besides inhibition of root apical meristem (RAM) activity under all stresses, As induced lateral root growth while root hair density and lengths were strongly increased by Hpx and HpxAs-treatments. A dual stimulation of phosphate (Pi)-starvation response was observed for HpxAstreated plant roots; however, the response under HpxAs aligned more with Hpx than As. Transcriptional evidence along with biochemical data suggests involvement of PHOSPHATE STARVATION RESPONSE 1; PHR1-dependent systemic signaling. Pi metabolism-related transcripts in close association with cellular iron homeostasis modulate root development under HpxAs. Early redox potential changes in meristematic cells, differential ROS accumulation in root hair zone cell layers and strong deregulation of NADPH oxidases, NADPH-dependent oxidoreductases and peroxidases signify a role of redox and ROS signaling in root architecture remodeling under HpxAs. Differential aquaporin expression suggests transmembrane ROS transport to regulate root hair induction and growth. Reorganization of energy metabolism through NO-dependent alternate oxidase, lactate fermentation, and phosphofructokinase seems crucial under HpxAs. TOR and SnRK-signaling network components were potentially involved in

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“…Studies in plants revealed a glucose-TOR signaling pathway that integrates light and sugar availability to control meristem activation in root and shoot (Li et al, 2017; Chen et al, 2018; Pfeiffer et al, 2016; Xiong et al, 2013), connecting TOR signaling to the generation and availability of photosynthates. A recent work identified isopropylmalate synthase 1 (IPMS1), a critical enzyme for Leu biosynthesis, as a suppressor of lrx1 , a mutant that is defective in root hair development (Schaufelberger et al, 2019). Additionally, this research found that mutation of IPMS1 affects root development by reducing its sensitivity to chemical inhibition of TOR (Schaufelberger et al, 2019), suggesting alteration of Leu biosynthesis modifies the TOR network.…”

Section: Introductionmentioning

confidence: 99%

“…A recent work identified isopropylmalate synthase 1 (IPMS1), a critical enzyme for Leu biosynthesis, as a suppressor of lrx1 , a mutant that is defective in root hair development (Schaufelberger et al, 2019). Additionally, this research found that mutation of IPMS1 affects root development by reducing its sensitivity to chemical inhibition of TOR (Schaufelberger et al, 2019), suggesting alteration of Leu biosynthesis modifies the TOR network. Therefore, the level of conservation of TOR signaling input across kingdoms and in plant cells specifically is still a significant question.…”

Section: Introductionmentioning

confidence: 99%

Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis

Cao

Kim

Xing

et al. 2019

eLife

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The target of rapamycin (TOR) kinase is an evolutionarily conserved hub of nutrient sensing and metabolic signaling. In plants, a functional connection of TOR activation with glucose availability was demonstrated, while it is yet unclear whether branched-chain amino acids (BCAAs) are a primary input of TOR signaling as they are in yeast and mammalian cells. Here, we report on the characterization of an Arabidopsis mutant over-accumulating BCAAs. Through chemical interventions targeting TOR and by examining mutants of BCAA biosynthesis and TOR signaling, we found that BCAA over-accumulation leads to up-regulation of TOR activity, which causes reorganization of the actin cytoskeleton and actin-associated endomembranes. Finally, we show that activation of TOR is concomitant with alteration of cell expansion, proliferation and specialized metabolism, leading to pleiotropic effects on plant growth and development. These results demonstrate that BCAAs contribute to plant TOR activation and reveal previously uncharted downstream subcellular processes of TOR signaling.

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Mutations in the Arabidopsis ROL17/isopropylmalate synthase 1 locus alter amino acid content, modify the TOR network, and suppress the root hair cell development mutant lrx1

Abstract: Interfering with leucine biosynthesis affects the TOR network and causes changes in cell growth that lead to suppression of the cell wall formation mutant lrx1 .

Cited by 36 publications

References 76 publications

Parallel global profiling of plant TOR dynamics reveals a conserved role for LARP1 in translation

Parallel global profiling of plant TOR dynamics reveals a conserved role for LARP1 in translation

Remodeling of Root Growth Under Combined Arsenic and Hypoxia Stress Is Linked to Nutrient Deprivation

Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis

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