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.

Data availability

The following data sets were generated

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

Version 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.

Metrics

  • 6,026
    views
  • 1,171
    downloads
  • 34
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Christophe Gaillochet
  2. Thomas Stiehl
  3. Christian Wenzl
  4. Juan-José Ripoll
  5. Lindsay J Bailey-Steinitz
  6. Lanxin Li
  7. Anne Pfeiffer
  8. Andrej Miotk
  9. Jana Hakenjos
  10. Joachim Forner
  11. Martin F Yanofsky
  12. Anna Marciniak-Czochra
  13. Jan U Lohmann
(2017)
Control of plant cell fate transitions by transcriptional and hormonal signals
eLife 6:e30135.
https://doi.org/10.7554/eLife.30135

Share this article

https://doi.org/10.7554/eLife.30135

Further reading

    1. Developmental Biology
    Edgar M Pera, Josefine Nilsson-De Moura ... Ivana Milas
    Research Article

    We previously showed that SerpinE2 and the serine protease HtrA1 modulate fibroblast growth factor (FGF) signaling in germ layer specification and head-to-tail development of Xenopus embryos. Here, we present an extracellular proteolytic mechanism involving this serpin-protease system in the developing neural crest (NC). Knockdown of SerpinE2 by injected antisense morpholino oligonucleotides did not affect the specification of NC progenitors but instead inhibited the migration of NC cells, causing defects in dorsal fin, melanocyte, and craniofacial cartilage formation. Similarly, overexpression of the HtrA1 protease impaired NC cell migration and the formation of NC-derived structures. The phenotype of SerpinE2 knockdown was overcome by concomitant downregulation of HtrA1, indicating that SerpinE2 stimulates NC migration by inhibiting endogenous HtrA1 activity. SerpinE2 binds to HtrA1, and the HtrA1 protease triggers degradation of the cell surface proteoglycan Syndecan-4 (Sdc4). Microinjection of Sdc4 mRNA partially rescued NC migration defects induced by both HtrA1 upregulation and SerpinE2 downregulation. These epistatic experiments suggest a proteolytic pathway by a double inhibition mechanism:

    SerpinE2 ┤HtrA1 protease ┤Syndecan-4 → NC cell migration.

    1. Developmental Biology
    2. Neuroscience
    Kristine B Walhovd, Stine K Krogsrud ... Didac Vidal-Pineiro
    Research Article

    Human fetal development has been associated with brain health at later stages. It is unknown whether growth in utero, as indexed by birth weight (BW), relates consistently to lifespan brain characteristics and changes, and to what extent these influences are of a genetic or environmental nature. Here we show remarkably stable and lifelong positive associations between BW and cortical surface area and volume across and within developmental, aging and lifespan longitudinal samples (N = 5794, 4–82 y of age, w/386 monozygotic twins, followed for up to 8.3 y w/12,088 brain MRIs). In contrast, no consistent effect of BW on brain changes was observed. Partly environmental effects were indicated by analysis of twin BW discordance. In conclusion, the influence of prenatal growth on cortical topography is stable and reliable through the lifespan. This early-life factor appears to influence the brain by association of brain reserve, rather than brain maintenance. Thus, fetal influences appear omnipresent in the spacetime of the human brain throughout the human lifespan. Optimizing fetal growth may increase brain reserve for life, also in aging.