1. Developmental Biology
  2. Plant Biology
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Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways

  1. Jenia Schlegel
  2. Gregoire Denay
  3. Rene H Wink
  4. Karine Gustavo Pinto
  5. Yvonne Stahl
  6. Julia Schmid
  7. Patrick Blümke
  8. Rüdiger GW Simon  Is a corresponding author
  1. Heinrich-Heine University, Germany
Research Article
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Cite this article as: eLife 2021;10:e70934 doi: 10.7554/eLife.70934

Abstract

Stem cell homeostasis in plant shoot meristems requires tight coordiantion between stem cell proliferation and cell differentiation. In Arabidopsis, stem cells express the secreted dodecapeptide CLAVATA3 (CLV3), which signals through the leucine-rich repeat (LRR)-receptor kinase CLAVATA1 (CLV1) and related CLV1-family members to downregulate expression of the homeodomain transcription factor WUSCHEL (WUS). WUS protein moves from cells below the stem cell domain to the meristem tip and promotes stem cell identity, together with CLV3 expression, generating a negative feedback loop. How stem cell activity in the meristem centre is coordinated with organ initiation and cell differentiation at the periphery is unknown. We show here that the CLE40 gene, encoding a secreted peptide closely related to CLV3, is expressed in the SAM in differentiating cells in a pattern complementary to that of CLV3. CLE40 promotes WUS expression via BAM1, a CLV1-family receptor, and CLE40 expression is in turn repressed in a WUS-dependent manner. Together, CLE40-BAM1-WUS establish a second negative feedback loop. We propose that stem cell homeostasis is achieved through two intertwined pathways that adjust WUS activity and incorporate information on the size of the stem cell domain, via CLV3-CLV1, and on cell differentiation via CLE40-BAM1.

Data availability

Original microscopy and image analysis data represented in the manuscript is available via Dryad (https://doi.org/10.5061/dryad.1g1jwstwf), all other experimental replicates are available at BioImage Archive (S-BSST723).

The following data sets were generated

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Author details

  1. Jenia Schlegel

    Heinrich-Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0434-4479

  2. Gregoire Denay

    Heinrich-Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8850-3029

  3. Rene H Wink

    Heinrich-Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.

  4. Karine Gustavo Pinto

    Heinrich-Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Yvonne Stahl

    Heinrich-Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.

  6. Julia Schmid

    Heinrich-Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.

  7. Patrick Blümke

    Heinrich-Heine University, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7315-6792

  8. Rüdiger GW Simon

    Heinrich-Heine University, Düsseldorf, Germany
    For correspondence
    ruediger.simon@hhu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1317-7716

Funding

Deutsche Forschungsgemeinschaft (iGRAD-PLANT,CEPLAS,SFB1208)

  • Gregoire Denay

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: June 2, 2021
  2. Preprint posted: June 16, 2021 (view preprint)
  3. Accepted: September 30, 2021
  4. Accepted Manuscript published: October 13, 2021 (version 1)
  5. Version of Record published: November 16, 2021 (version 2)

Copyright

© 2021, Schlegel 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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