Cell cycle control by the target of rapamycin signalling pathway in plants

Ahmad, Zaki; Magyar, Zoltán; Bögre, László; Papdi, Csaba

doi:10.1093/jxb/erz140

Cited by 29 publications

(26 citation statements)

References 99 publications

(129 reference statements)

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“…Adding to this complex network, we found that regulators of cell division and cyclin expression that are involved in developmental patterning, including the transcription factor PEAPOD2 (PPD2) ( Baekelandt et al, 2018 ; White, 2006 ) and several proteins involved in auxin signaling, which has previously been reported to act upstream of TOR ( Beltrán-Peña et al, 2002 ; Chen et al, 2018a ; Li et al, 2017b ; Schepetilnikov et al, 2017 ; Turck et al, 2004 ), are encoded by TOR-LARP1-5′TOP-regulated mRNAs. Ongoing investigations of the role of TOR in cell cycle regulation could elucidate the relative contributions of the transcriptional, translational, and post-translational regulatory steps in this multilayered TOR signaling network ( Ahmad et al, 2019 ; Lokdarshi et al, 2020 ).…”

Section: Discussionmentioning

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: Discussionmentioning

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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“…Because many recent reviews have summarized the status of plant TOR signaling in detail (Ahmad, Magyar, Bogre, & Papdi, 2019;Caldana, Martins, Mubeen, & Urrea-Castellanos, 2019;M. Rodriguez, Parola, Andreola, Pereyra, & Martinez-Noel, 2019;Schepetilnikov & Ryabova, 2018;Sesma, Castresana, & Castellano, 2017;Shi et al, 2018) this section will focus on effects of TOR on the translation apparatus, building on the early observation that silencing of TOR inhibits mRNA-ribosome loading (Deprost et al, 2007).…”

Section: Tor Kinase Signalingmentioning

confidence: 99%

Translational gene regulation in plants: A green new deal

2020

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The molecular machinery for protein synthesis is profoundly similar between plants and other eukaryotes. Mechanisms of translational gene regulation are embedded into the broader network of RNA-level processes including RNA quality control and RNA turnover. However, over eons of their separate history, plants acquired new components, dropped others, and generally evolved an alternate way of making the parts list of protein synthesis work. Research over the past 5 years has unveiled how plants utilize translational control to defend themselves against viruses, regulate translation in response to metabolites, and reversibly adjust translation to a wide variety of environmental parameters. Moreover, during seed and pollen development plants make use of RNA granules and other translational controls to underpin developmental transitions between quiescent and metabolically active stages. The economics of resource allocation over the daily light-dark cycle also include controls over cellular protein synthesis. Important new insights into translational control on cytosolic ribosomes continue to emerge from studies of translational control mechanisms in viruses. Finally, sketches of coherent signaling pathways that connect external stimuli with a translational response are emerging, anchored in part around TOR and GCN2 kinase signaling networks. These again reveal some mechanisms that are familiar and others that are different from other eukaryotes, motivating deeper studies on translational control in plants.

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“…Therefore, we propose that TOR translationally controls expression of cyclins to promote cell cycle progression, in addition to regulation of YAK1 upstream (Forzani et al, 2019) and E2Fa downstream of cyclin-CDK-RBR1 signaling. Ongoing investigations of the role of TOR in cell cycle regulation could elucidate the relative contributions of the transcriptional, translational, and post-translational regulatory steps in this multilayered TOR signaling network (Ahmad et al, 2019;Lokdarshi et al, 2020).…”

Section: Multilayered Regulation Of Plant Cell Cycle Progression By Tormentioning

confidence: 99%

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

Scarpin

Leiboff

Brunkard

2020

Preprint

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Author ContributionsAll authors contributed to the design, execution, and analysis of experiments. S.L. specifically contributed to the design and computational analysis of RNA sequencing experiments. M.R.S. and J.O.B. wrote the manuscript. ABSTRACTTARGET OF RAPAMYCIN (TOR) is a deeply conserved protein kinase that coordinates eukaryotic metabolism with nutrient availability. 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.Here, we took parallel global profiling approaches to define the in planta 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 the canonical 5′ oligopyrimidine tract motif (5′TOP) found in mammalian ribosomal protein mRNAs. To investigate this further, we focused on a putative TOR substrate identified in our phosphoproteome: LARP1, a eukaryotic RNAbinding protein that is proposed to mediate TOR translational control of 5′TOP mRNAs in humans and that has gained increased interest because it associates with SARS-CoV-2. By conducting parallel global profiling experiments with larp1 mutants, we discovered that the TOR-LARP1 signaling axis controls 5′TOP mRNA translation in plants and defined a set of conserved eukaryotic 5′TOP mRNAs that encode cyclins, importins/karyopherins, translation elongation factors, and TCTP1, among others. We then identified novel, plantspecific 5′TOP mRNAs involved in critical biological processes, including ribosome biogenesis, chromatin remodeling, and auxin signaling. Our study illuminates the ancestral roles of the TOR-LARP1-5′TOP metabolic regulatory network and provides evolutionary context for ongoing debates about the molecular function of LARP1 in eukaryotic cells.

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Cell cycle control by the target of rapamycin signalling pathway in plants

Cited by 29 publications

References 99 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

Translational gene regulation in plants: A green new deal

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

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