Autocrine regulation of stomatal differentiation potential by EPF1 and ERECTA-LIKE1 ligand-receptor signaling

  1. Xingyun Qi
  2. Soon-Ki Han
  3. Jonathan H Dang
  4. Jacqueline M Garrick
  5. Masaki Ito
  6. Alexander K Hofstetter
  7. Keiko U Torii  Is a corresponding author
  1. Howard Hughes Medical Institute, University of Washington, United States
  2. Nagoya University, Japan

Abstract

Development of stomata, valves on the plant epidermis for optimal gas exchange and water control, is fine-tuned by multiple signaling peptides with unique, overlapping, or antagonistic activities. EPIDERMAL PATTERNING FACTOR1 (EPF1) is a founding member of the secreted peptide ligands enforcing stomatal patterning. Yet, its exact role remains unclear. Here, we report that EPF1 and its primary receptor ERECTA-LIKE1 (ERL1) target MUTE, a transcription factor specifying the proliferation-to-differentiation switch within the stomatal cell lineages. In turn, MUTE directly induces ERL1. The absolute co-expression of ERL1 and MUTE, with the co-presence of EPF1, triggers autocrine inhibition of stomatal fate. During normal stomatal development, this autocrine inhibition prevents extra symmetric divisions of stomatal precursors likely owing to excessive MUTE activity. Our study reveals the unexpected role of self-inhibition as a mechanism for ensuring proper stomatal development and suggests an intricate signal buffering mechanism underlying plant tissue patterning.

Article and author information

Author details

  1. Xingyun Qi

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Soon-Ki Han

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jonathan H Dang

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jacqueline M Garrick

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Masaki Ito

    Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexander K Hofstetter

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Keiko U Torii

    Howard Hughes Medical Institute, University of Washington, Seattle, United States
    For correspondence
    ktorii@u.washington.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

  • Keiko U Torii

Gordon and Betty Moore Foundation (GBMF3035)

  • Keiko U Torii

National Science Foundation (MCB-0855659)

  • 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. Sheila McCormick, University of California-Berkeley, United States

Publication history

  1. Received: December 9, 2016
  2. Accepted: March 6, 2017
  3. Accepted Manuscript published: March 7, 2017 (version 1)
  4. Accepted Manuscript updated: March 14, 2017 (version 2)
  5. Version of Record published: March 20, 2017 (version 3)

Copyright

© 2017, 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. Soon-Ki Han
  3. Jonathan H Dang
  4. Jacqueline M Garrick
  5. Masaki Ito
  6. Alexander K Hofstetter
  7. Keiko U Torii
(2017)
Autocrine regulation of stomatal differentiation potential by EPF1 and ERECTA-LIKE1 ligand-receptor signaling
eLife 6:e24102.
https://doi.org/10.7554/eLife.24102
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