The manifold actions of signaling peptides on subcellular dynamics of a receptor specify stomatal cell fate

  1. Xingyun Qi
  2. Akira Yoshinari
  3. Pengfei Bai
  4. Michal Maes
  5. Scott M Zeng
  6. Keiko U Torii  Is a corresponding author
  1. Unversity of Washington, United States
  2. Nagoya University, Japan
  3. University of Texas at Austin, United States
  4. University of Washington, United States

Abstract

Receptor endocytosis is important for signal activation, transduction, and deactivation. However, how a receptor interprets conflicting signals to adjust cellular output is not clearly understood. Using genetic, cell biological, and pharmacological approaches, we report here that ERECTA-LIKE1 (ERL1), the major receptor restricting plant stomatal differentiation, undergoes dynamic subcellular behaviors in response to different EPIDERMAL PATTERNING FACTOR (EPF) peptides. Activation of ERL1 by EPF1 induces rapid ERL1 internalization via multivesicular bodies/late endosomes to vacuolar degradation, whereas ERL1 constitutively internalizes in the absence of EPF1. The co-receptor, TOO MANY MOUTHS is essential for ERL1 internalization induced by EPF1 but not by EPFL6. The peptide antagonist, Stomagen, triggers retention of ERL1 in the endoplasmic reticulum, likely coupled with reduced endocytosis. In contrast, the dominant-negative ERL1 remained dysfunctional in ligand-induced subcellular trafficking. Our study elucidates that multiple related yet unique peptides specify cell fate by deploying the differential subcellular dynamics of a single receptor.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source R codes are provided.

Article and author information

Author details

  1. Xingyun Qi

    Biology, Unversity of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Akira Yoshinari

    Institute of Transformative Biomolecules, Nagoya University, Nagoya, Aichi, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Pengfei Bai

    Molecular Biosciences, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Michal Maes

    Biology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Scott M Zeng

    Physics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Keiko U Torii

    Molecular Biosciences, University of Texas at Austin, Austin, United States
    For correspondence
    ktorii@utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6168-427X

Funding

Howard Hughes Medical Institute (TORII)

  • Keiko U Torii

Gordon and Betty Moore Foundation (GBMF3035)

  • Keiko U Torii

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

Reviewing Editor

  1. Jürgen Kleine-Vehn, University of Natural Resources and Life Sciences, Austria

Publication history

  1. Received: April 21, 2020
  2. Accepted: August 14, 2020
  3. Accepted Manuscript published: August 14, 2020 (version 1)
  4. Version of Record published: September 3, 2020 (version 2)

Copyright

© 2020, Qi 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. Xingyun Qi
  2. Akira Yoshinari
  3. Pengfei Bai
  4. Michal Maes
  5. Scott M Zeng
  6. Keiko U Torii
(2020)
The manifold actions of signaling peptides on subcellular dynamics of a receptor specify stomatal cell fate
eLife 9:e58097.
https://doi.org/10.7554/eLife.58097

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