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

Research Article
  • Cited 21
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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.

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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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Further reading

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    2. Stem Cells and Regenerative Medicine
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    The gut is the primary interface between an animal and food, but how it adapts to qualitative dietary variation is poorly defined. We find that the Drosophila midgut plastically resizes following changes in dietary composition. A panel of nutrients collectively promote gut growth, which sugar opposes. Diet influences absolute and relative levels of enterocyte loss and stem cell proliferation, which together determine cell numbers. Diet also influences enterocyte size. A high sugar diet inhibits translation and uncouples ISC proliferation from expression of niche-derived signals but, surprisingly, rescuing these effects genetically was not sufficient to modify diet's impact on midgut size. However, when stem cell proliferation was deficient, diet's impact on enterocyte size was enhanced, and reducing enterocyte-autonomous TOR signaling was sufficient to attenuate diet-dependent midgut resizing. These data clarify the complex relationships between nutrition, epithelial dynamics, and cell size, and reveal a new mode of plastic, diet-dependent organ resizing.

    1. Developmental Biology
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    Research Article Updated

    Spatial boundaries formed during animal development originate from the pre-patterning of tissues by signaling molecules, called morphogens. The accuracy of boundary location is limited by the fluctuations of morphogen concentration that thresholds the expression level of target gene. Producing more morphogen molecules, which gives rise to smaller relative fluctuations, would better serve to shape more precise target boundaries; however, it incurs more thermodynamic cost. In the classical diffusion-depletion model of morphogen profile formation, the morphogen molecules synthesized from a local source display an exponentially decaying concentration profile with a characteristic length λ. Our theory suggests that in order to attain a precise profile with the minimal cost, λ should be roughly half the distance to the target boundary position from the source. Remarkably, we find that the profiles of morphogens that pattern the Drosophila embryo and wing imaginal disk are formed with nearly optimal λ. Our finding underscores the cost-effectiveness of precise morphogen profile formation in Drosophila development.