Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium

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 differenti...

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Main Authors: Elvira Hernandez-Lagana, Gabriella Mosca, Ethel Mendocilla-Sato, Nuno Pires, Anja Frey, Alejandro Giraldo-Fonseca, Caroline Michaud, Ueli Grossniklaus, Olivier Hamant, Christophe Godin, Arezki Boudaoud, Daniel Grimanelli, Daphné Autran, Célia Baroux
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/66031
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author Elvira Hernandez-Lagana
Gabriella Mosca
Ethel Mendocilla-Sato
Nuno Pires
Anja Frey
Alejandro Giraldo-Fonseca
Caroline Michaud
Ueli Grossniklaus
Olivier Hamant
Christophe Godin
Arezki Boudaoud
Daniel Grimanelli
Daphné Autran
Célia Baroux
author_facet Elvira Hernandez-Lagana
Gabriella Mosca
Ethel Mendocilla-Sato
Nuno Pires
Anja Frey
Alejandro Giraldo-Fonseca
Caroline Michaud
Ueli Grossniklaus
Olivier Hamant
Christophe Godin
Arezki Boudaoud
Daniel Grimanelli
Daphné Autran
Célia Baroux
author_sort Elvira Hernandez-Lagana
collection DOAJ
description 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.
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spelling doaj.art-b31fd24348464445b8e9342d4481f2d12022-12-22T02:01:56ZengeLife Sciences Publications LtdeLife2050-084X2021-05-011010.7554/eLife.66031Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordiumElvira Hernandez-Lagana0https://orcid.org/0000-0002-2645-3783Gabriella Mosca1https://orcid.org/0000-0003-4509-498XEthel Mendocilla-Sato2https://orcid.org/0000-0003-0339-3535Nuno Pires3https://orcid.org/0000-0002-7113-3519Anja Frey4Alejandro Giraldo-Fonseca5Caroline Michaud6https://orcid.org/0000-0002-0620-2442Ueli Grossniklaus7https://orcid.org/0000-0002-0522-8974Olivier Hamant8https://orcid.org/0000-0001-6906-6620Christophe Godin9https://orcid.org/0000-0002-1202-8460Arezki Boudaoud10https://orcid.org/0000-0002-2780-4717Daniel Grimanelli11https://orcid.org/0000-0001-5424-114XDaphné Autran12https://orcid.org/0000-0002-5227-8966Célia Baroux13https://orcid.org/0000-0001-6307-2229DIADE, University of Montpellier, CIRAD, IRD, Montpellier, FranceDepartment of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zürich, Zürich, SwitzerlandDepartment of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zürich, Zürich, SwitzerlandDepartment of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zürich, Zürich, SwitzerlandDepartment of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zürich, Zürich, SwitzerlandDepartment of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zürich, Zürich, SwitzerlandDIADE, University of Montpellier, CIRAD, IRD, Montpellier, FranceDepartment of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zürich, Zürich, SwitzerlandLaboratoire Reproduction et Développement des Plantes, University of Lyon, ENS Lyon, UCB Lyon 1, CNRS, INRAE, INRIA, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, University of Lyon, ENS Lyon, UCB Lyon 1, CNRS, INRAE, INRIA, Lyon, FranceLaboratoire Reproduction et Développement des Plantes, University of Lyon, ENS Lyon, UCB Lyon 1, CNRS, INRAE, INRIA, Lyon, FranceDIADE, University of Montpellier, CIRAD, IRD, Montpellier, FranceDIADE, University of Montpellier, CIRAD, IRD, Montpellier, France; Laboratoire Reproduction et Développement des Plantes, University of Lyon, ENS Lyon, UCB Lyon 1, CNRS, INRAE, INRIA, Lyon, FranceDepartment of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zürich, Zürich, SwitzerlandIn 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.https://elifesciences.org/articles/66031ovule primordiumgermlinecell fateplasticitygrowthtissue geometry
spellingShingle Elvira Hernandez-Lagana
Gabriella Mosca
Ethel Mendocilla-Sato
Nuno Pires
Anja Frey
Alejandro Giraldo-Fonseca
Caroline Michaud
Ueli Grossniklaus
Olivier Hamant
Christophe Godin
Arezki Boudaoud
Daniel Grimanelli
Daphné Autran
Célia Baroux
Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
eLife
ovule primordium
germline
cell fate
plasticity
growth
tissue geometry
title Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
title_full Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
title_fullStr Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
title_full_unstemmed Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
title_short Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
title_sort organ geometry channels reproductive cell fate in the arabidopsis ovule primordium
topic ovule primordium
germline
cell fate
plasticity
growth
tissue geometry
url https://elifesciences.org/articles/66031
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