Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium

  1. Elvira Hernandez-Lagana
  2. Gabriella Mosca
  3. Ethel Mendocilla-Sato
  4. Nuno Pires
  5. Anja Frey
  6. Alejandro Giraldo-Fonseca
  7. Caroline Michaud
  8. Ueli Grossniklaus
  9. Olivier Hamant
  10. Christophe Godin
  11. Arezki Boudaoud
  12. Daniel Grimanelli
  13. Daphné Autran  Is a corresponding author
  14. Célia Baroux  Is a corresponding author
  1. IRD, CIRAD, France
  2. University of Zürich, Switzerland
  3. Institut de Recherche pour le Développement, France
  4. Université de Lyon, ENS de Lyon, France
  5. University of Lyon, ENS Lyon, UCB Lyon 1, CNRS, INRAE, INRIA, France

Abstract

In multicellular organisms, sexual reproduction requires the separation of the germline from the soma. In flowering plants, the female germline precursor differentiates as a single spore mother cell (SMC) as the ovule primordium forms. Here, we explored how organ growth contributes to SMC differentiation. We generated 92 annotated 3D images at cellular resolution in Arabidopsis. We identified the spatio-temporal pattern of cell division that acts in a domain-specific manner as the primordium forms. Tissue growth models uncovered plausible morphogenetic principles involving a spatially confined growth signal, differential mechanical properties, and cell growth anisotropy. Our analysis revealed that SMC characteristics first arise in more than one cell but SMC fate becomes progressively restricted to a single cell during organ growth. Altered primordium geometry coincided with a delay in the fate restriction process in katanin mutants. Altogether, our study suggests that tissue geometry channels reproductive cell fate in the Arabidopsis ovule primordium.

Data availability

The data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all Figures. Segmented Image data are deposited in Dryad Digital Repository, available at: doi:10.5061/dryad.02v6wwq2c. Cell Statistics from these images are deposited as 'Segmented Dataset ...csv' at https://github.com/barouxlab/OvuleViz

The following data sets were generated

Article and author information

Author details

  1. Elvira Hernandez-Lagana

    DIADE, IRD, CIRAD, Montpellier, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2645-3783
  2. Gabriella Mosca

    Plant and Microbial Biology, University of Zürich, Zürich, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4509-498X
  3. Ethel Mendocilla-Sato

    Plant and Microbial Biology, University of Zürich, Zürich, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0339-3535
  4. Nuno Pires

    Plant and Microbial Biology, University of Zürich, Zürich, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7113-3519
  5. Anja Frey

    Plant and Microbial Biology, University of Zürich, Zürich, Switzerland
    Competing interests
    Anja Frey, Anja Frey is affiliated with Novartis Pharma Schweiz AG. The author has no financial interests to declare.
  6. Alejandro Giraldo-Fonseca

    Plant and Microbial Biology, University of Zürich, Zürich, Switzerland
    Competing interests
    No competing interests declared.
  7. Caroline Michaud

    DIADE, Institut de Recherche pour le Développement, Montpellier, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0620-2442
  8. Ueli Grossniklaus

    Plant and Microbial Biology, University of Zürich, Zürich, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0522-8974
  9. Olivier Hamant

    Laboratoire de Reproduction de développement des plantes, Institut national de la recherche agronomique, Centre national de la recherche scientifique, ENS Lyon, Claude Bernard University Lyon, Université de Lyon, ENS de Lyon, Lyon, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6906-6620
  10. Christophe Godin

    Laboratoire de Reproduction de développement des plantes, Institut national de la recherche agronomique, Centre national de la recherche scientifique, ENS Lyon, Claude Bernard University Lyon, University of Lyon, ENS Lyon, UCB Lyon 1, CNRS, INRAE, INRIA, Lyon, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1202-8460
  11. Arezki Boudaoud

    Laboratoire de Reproduction de développement des plantes, Institut national de la recherche agronomique, Centre national de la recherche scientifique, ENS Lyon, Claude Bernard University Lyon, Université de Lyon, ENS de Lyon, Lyon, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2780-4717
  12. Daniel Grimanelli

    DIADE, IRD, CIRAD, Montpellier, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5424-114X
  13. Daphné Autran

    DIADE, Institut de Recherche pour le Développement, Montpellier, France
    For correspondence
    daphne.autran@ird.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5227-8966
  14. Célia Baroux

    Plant and Microbial Biology, University of Zürich, Zürich, Switzerland
    For correspondence
    cbaroux@botinst.uzh.ch
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6307-2229

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030L_170167)

  • Célia Baroux

Agence Nationale de la Recherche (16-CE93-0002)

  • Daphné Autran

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030B_160336)

  • Ueli Grossniklaus

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (IZCOZ0_182949)

  • Célia Baroux

Kommission für Technologie und Innovation (16997)

  • Célia Baroux

Baugarten Stiftung

  • Célia Baroux

Consejo Nacional de Ciencia y Tecnología (438277)

  • Elvira Hernandez-Lagana

Forschungskredit Universitaet Zuerich (FK-74502-04-01)

  • Gabriella Mosca

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 22, 2020
  2. Accepted: May 3, 2021
  3. Accepted Manuscript published: May 7, 2021 (version 1)
  4. Version of Record published: June 22, 2021 (version 2)

Copyright

© 2021, Hernandez-Lagana 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. Elvira Hernandez-Lagana
  2. Gabriella Mosca
  3. Ethel Mendocilla-Sato
  4. Nuno Pires
  5. Anja Frey
  6. Alejandro Giraldo-Fonseca
  7. Caroline Michaud
  8. Ueli Grossniklaus
  9. Olivier Hamant
  10. Christophe Godin
  11. Arezki Boudaoud
  12. Daniel Grimanelli
  13. Daphné Autran
  14. Célia Baroux
(2021)
Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
eLife 10:e66031.
https://doi.org/10.7554/eLife.66031

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