TARGET 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
(5TOP) found in mammalian ribosomal protein mRNAs. To investigate this further, we
focused on a putative TOR substrate identified in our phosphoproteome: LARP1, a
eukaryotic RNA-binding protein that is proposed to mediate TOR translational control of
5TOP 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 5TOP mRNA
translation in plants and defined a set of conserved eukaryotic 5TOP mRNAs that
encode cyclins, importins/karyopherins, translation elongation factors, and TCTP1,
among others. We then identified novel, plant-specific 5TOP mRNAs involved in critical
biological processes, including ribosome biogenesis, chromatin remodeling, and auxin
signaling. Our study illuminates the ancestral roles of the TOR-LARP1-5TOP metabolic
regulatory network and provides evolutionary context for ongoing debates about the
molecular function of LARP1 in eukaryotic cells. Less...