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

Publication 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.

Metrics

  • 2,247
    Page views
  • 358
    Downloads
  • 13
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Cell Biology
    Tai-De Li et al.
    Research Article

    Branched actin networks are self-assembling molecular motors that move biological membranes and drive many important cellular processes, including phagocytosis, endocytosis, and pseudopod protrusion. When confronted with opposing forces, the growth rate of these networks slows and their density increases, but the stoichiometry of key components does not change. The molecular mechanisms governing this force response are not well understood, so we used single-molecule imaging and AFM cantilever deflection to measure how applied forces affect each step in branched actin network assembly. Although load forces are observed to increase the density of growing filaments, we find that they actually decrease the rate of filament nucleation due to inhibitory interactions between actin filament ends and nucleation promoting factors. The force-induced increase in network density turns out to result from an exponential drop in the rate constant that governs filament capping. The force dependence of filament capping matches that of filament elongation and can be explained by expanding Brownian Ratchet theory to cover both processes. We tested a key prediction of this expanded theory by measuring the force-dependent activity of engineered capping protein variants and found that increasing the size of the capping protein increases its sensitivity to applied forces. In summary, we find that Brownian Ratchets underlie not only the ability of growing actin filaments to generate force but also the ability of branched actin networks to adapt their architecture to changing loads.

    1. Cell Biology
    2. Immunology and Inflammation
    Ekaterini Maria Lyras et al.
    Research Article

    The tongue is a unique muscular organ situated in the oral cavity where it is involved in taste sensation, mastication, and articulation. As a barrier organ, which is constantly exposed to environmental pathogens, the tongue is expected to host an immune cell network ensuring local immune defence. However, the composition and the transcriptional landscape of the tongue immune system are currently not completely defined. Here, we characterised the tissue-resident immune compartment of the murine tongue during development, health and disease, combining single-cell RNA-sequencing with in situ immunophenotyping. We identified distinct local immune cell populations and described two specific subsets of tongue-resident macrophages occupying discrete anatomical niches. Cx3cr1+ macrophages were located specifically in the highly innervated lamina propria beneath the tongue epidermis and at times in close proximity to fungiform papillae. Folr2+ macrophages were detected in deeper muscular tissue. In silico analysis indicated that the two macrophage subsets originate from a common proliferative precursor during early postnatal development and responded differently to systemic LPS in vivo. Our description of the under-investigated tongue immune system sets a starting point to facilitate research on tongue immune-physiology and pathology including cancer and taste disorders.