Parallel global profiling of plant TOR dynamics

TARGET OF RAPAMYCIN (TOR) is a deeply conserved protein kinase thatcoordinates eukaryotic metabolism with nutrient availability. In mammals, TORspecifically promotes translation of ribosomal protein mRNAs when amino acids areavailable to support protein synthesis. The mechanisms controlling translationdownstream from TOR remain contested, however, and are largely unexplored inplants. Here, we took parallel global profiling approaches to define the in planta TOR-regulated transcriptome, translatome, proteome, and phosphoproteome. We found thatTOR regulates ribosome biogenesis in plants at multiple levels, but throughmechanisms that do not directly depend on the canonical 5 oligopyrimidine tract motif(5TOP) found in mammalian ribosomal protein mRNAs. To investigate this further, wefocused on a putative TOR substrate identified in our phosphoproteome: LARP1, aeukaryotic RNA-binding protein that is proposed to mediate TOR translational control of5TOP mRNAs in humans and that has gained increased interest because it associateswith SARS-CoV-2. By conducting parallel global profiling experiments with larp1mutants, we discovered that the TOR-LARP1 signaling axis controls 5TOP mRNAtranslation in plants and defined a set of conserved eukaryotic 5TOP mRNAs thatencode cyclins, importins/karyopherins, translation elongation factors, and TCTP1,among others. We then identified novel, plant-specific 5TOP mRNAs involved in criticalbiological processes, including ribosome biogenesis, chromatin remodeling, and auxinsignaling. Our study illuminates the ancestral roles of the TOR-LARP1-5TOP metabolicregulatory network and provides evolutionary context for ongoing debates about themolecular function of LARP1 in eukaryotic cells.