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

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Abstract

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.

Data availability

Sequencing data are available at NCBI SRA, project PRJNA639161.Proteome data are available via PRIDE and ProteomeXchange, doi:10.6019/PXD019942.

The following data sets were generated

(2020) Parallel global profiling of plant TOR dynamics
NCBI SRA, PRJNA639161.

https://www.ncbi.nlm.nih.gov/sra/PRJNA639161
(2020) Parallel global profiling of plant TOR dynamics
PRIDE, PXD019942.

https://doi.org/10.6019/PXD019942

Article and author information

Author details

M Regina Scarpin

Plant and Microbial Biology, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.
Samuel Leiboff

Botany and Plant Pathology, Oregon State University, Corvallis, United States

Competing interests
The authors declare that no competing interests exist.
Jacob Oliver Brunkard

Laboratory of Genetics, University of Wisconsin, Madison, Madison, United States

For correspondence
brunkard@berkeley.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6407-9393

Funding

National Institutes of Health (DP5-OD023072)

Jacob Oliver Brunkard

National Science Foundation (IOS-1612268)

Samuel Leiboff

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.