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

  1. M Regina Scarpin
  2. Samuel Leiboff
  3. Jacob Oliver Brunkard  Is a corresponding author
  1. University of California, Berkeley, United States
  2. Oregon State University, United States
  3. University of Wisconsin, Madison, United States

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

Article and author information

Author details

  1. M Regina Scarpin

    Plant and Microbial Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Samuel Leiboff

    Botany and Plant Pathology, Oregon State University, Corvallis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. 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.
    ORCID icon "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.

Reviewing Editor

  1. Nahum Sonenberg, McGill University, Canada

Version history

  1. Received: May 13, 2020
  2. Accepted: October 14, 2020
  3. Accepted Manuscript published: October 15, 2020 (version 1)
  4. Version of Record published: October 23, 2020 (version 2)

Copyright

© 2020, Scarpin et al.

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.

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  1. M Regina Scarpin
  2. Samuel Leiboff
  3. Jacob Oliver Brunkard
(2020)
Parallel global profiling of plant TOR dynamics reveals a conserved role for LARP1 in translation
eLife 9:e58795.
https://doi.org/10.7554/eLife.58795

Share this article

https://doi.org/10.7554/eLife.58795

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