1. Developmental Biology
  2. Plant Biology
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Control of plant cell fate transitions by transcriptional and hormonal signals

Research Article
  • Cited 19
  • Views 4,896
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Cite this article as: eLife 2017;6:e30135 doi: 10.7554/eLife.30135

Abstract

Plant meristems carry pools of continuously active stem cells, whose activity is controlled by developmental and environmental signals. After stem cell division, daughter cells that exit the stem cell domain acquire transit amplifying cell identity before they are incorporated into organs and differentiate. In this study, we used an integrated approach to elucidate the role of HECATE (HEC) genes in regulating developmental trajectories of shoot stem cells in Arabidopsis thaliana. Our work reveals that HEC function stabilizes cell fate in distinct zones of the shoot meristem thereby controlling the spatio-temporal dynamics of stem cell differentiation. Importantly, this activity is concomitant with the local modulation of cellular responses to cytokinin and auxin, two key phytohormones regulating cell behaviour. Mechanistically, we show that HEC factors transcriptionally control and physically interact with MONOPTEROS (MP), a key regulator of auxin signalling, and modulate the autocatalytic stabilization of auxin signalling output.

Article and author information

Author details

  1. Christophe Gaillochet

    Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Thomas Stiehl

    Institute of Applied Mathematics, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Christian Wenzl

    Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Juan-José Ripoll

    Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8229-1555
  5. Lindsay J Bailey-Steinitz

    Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Lanxin Li

    Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Anne Pfeiffer

    Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Andrej Miotk

    Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2581-672X
  9. Jana Hakenjos

    Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Joachim Forner

    Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6406-7066
  11. Martin F Yanofsky

    Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Anna Marciniak-Czochra

    Institute of Applied Mathematics, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Jan U Lohmann

    Department of Stem Cell Biology, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    For correspondence
    jan.lohmann@cos.uni-heidelberg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3667-187X

Funding

Deutsche Forschungsgemeinschaft (SFB873)

  • Anna Marciniak-Czochra
  • Jan U Lohmann

European Social Fund (Elite programm für Postdocs)

  • Anne Pfeiffer

Baden-Württemberg Stiftung (Elite programm für Postdocs)

  • Anne Pfeiffer

National Institutes of Health (1R01GM112976-01A1)

  • Martin F Yanofsky

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

Reviewing Editor

  1. Dominique C Bergmann, Stanford University/HHMI, United States

Publication history

  1. Received: July 3, 2017
  2. Accepted: October 22, 2017
  3. Accepted Manuscript published: October 23, 2017 (version 1)
  4. Accepted Manuscript updated: October 24, 2017 (version 2)
  5. Accepted Manuscript updated: October 26, 2017 (version 3)
  6. Version of Record published: November 17, 2017 (version 4)

Copyright

© 2017, Gaillochet 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. Further reading

Further reading

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    A notable example of spiral architecture in organs is the mammalian cochlear duct, where the morphology is critical for hearing function. Genetic studies have revealed necessary signaling molecules, but it remains unclear how cellular dynamics generate elongating, bending, and coiling of the cochlear duct. Here, we show that extracellular signal-regulated kinase (ERK) activation waves control collective cell migration during the murine cochlear duct development using deep tissue live-cell imaging, Förster resonance energy transfer (FRET)-based quantitation, and mathematical modeling. Long-term FRET imaging reveals that helical ERK activation propagates from the apex duct tip concomitant with the reverse multicellular flow on the lateral side of the developing cochlear duct, resulting in advection-based duct elongation. Moreover, model simulations, together with experiments, explain that the oscillatory wave trains of ERK activity and the cell flow are generated by mechanochemical feedback. Our findings propose a regulatory mechanism to coordinate the multicellular behaviors underlying the duct elongation during development.