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

M Regina Scarpin,Jacob O Brunkard,Samuel Leiboff

doi:10.7554/elife.58795

Abstract

Target of rapamycin (TOR) is a protein kinase that coordinates eukaryotic metabolism. In mammals, TOR specifically promotes translation of ribosomal protein (RP) 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 RP 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.

Highlights

TARGET OF RAPAMYCIN (TOR) is a conserved eukaryotic serine/threonine protein kinase that regulates metabolism by promoting anabolic processes when nutrients are available (Liu and Sabatini, 2020)
We propose that TOR-La-related protein 1 (LARP1)-5′ terminal oligopyrimidine tract (5′TOP) mRNA signaling arose early during eukaryotic evolution to coordinate protein translation and cell division with cellular metabolic status and nutrient availability, and we argue that TOR-LARP1-5′TOP signaling has since evolved new, plant-specific targets that regulate plant physiology, growth, and development
To elucidate how LARP1 acts downstream of TOR, we repeated our global profiling experiments in larp1 mutants. Analysis of these results revealed that TOR-LARP1 signaling controls the translation of a specific set of mRNAs that begin with a 5′TOP motif, demonstrating that TOR-LARP1-5′TOP signaling is an ancestral function of the TOR signaling network in eukaryotes

Summary

Introduction

TARGET OF RAPAMYCIN (TOR) is a conserved eukaryotic serine/threonine protein kinase that regulates metabolism by promoting anabolic processes when nutrients are available (Liu and Sabatini, 2020). Many details of the TOR signaling pathway have been elucidated in mammals and yeast; less is known, about the TOR network in other eukaryotic lineages. When plant TOR is active, it promotes the transcription of genes involved in cell cycle progression, ribosome biogenesis, and various other metabolic processes, depending on developmental context (Xiong et al, 2013). Very little is understood about the signal transduction networks downstream from TOR in plants; elucidating these signaling pathways is a major goal to understand how TOR signaling evolved in eukaryotes and how TOR signaling networks could be manipulated to promote agricultural yields while reducing reliance on expensive and environmentally-harmful fertilizer inputs (Busche et al, 2020)

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