Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
- IRD, CIRAD, France
- University of Zürich, Switzerland
- Institut de Recherche pour le Développement, France
- Université de Lyon, ENS de Lyon, France
- 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
-
Arabidopsis ovule primordium stages 0-I to 2-II, wild-type Col_0, Ws-4 and botero (bot1-7) mutantDryad Digital Repository, doi:10.5061/dryad.02v6wwq2c.
-
Segmented_Dataset_Hernandez_Mosca_etal_2020https://github.com/barouxlab/OvuleViz.
Article and author information
Author details
Elvira Hernandez-Lagana
Ethel Mendocilla-Sato
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.
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.
Metrics
-
- 2,633
- views
-
- 468
- downloads
-
- 27
- 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)
Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium
eLife 10:e66031.
https://doi.org/10.7554/eLife.66031
Further reading
-
- Cell Biology
- Developmental Biology
The formation of large endolysosomal structures in unfertilized eggs ensures that lysosomes remain dormant before fertilization, and then shift into clean-up mode after the egg-to-embryo transition.
-
- Developmental Biology
Ribonucleoprotein (RNP) granules are membraneless electron-dense structures rich in RNAs and proteins, and involved in various cellular processes. Two RNP granules in male germ cells, intermitochondrial cement and the chromatoid body (CB), are associated with PIWI-interacting RNAs (piRNAs) and are required for transposon silencing and spermatogenesis. Other RNP granules in male germ cells, the reticulated body and CB remnants, are also essential for spermiogenesis. In this study, we disrupted FBXO24, a testis-enriched F-box protein, in mice and found numerous membraneless electron-dense granules accumulated in sperm flagella. Fbxo24 knockout (KO) mice exhibited malformed flagellar structures, impaired sperm motility, and male infertility, likely due to the accumulation of abnormal granules. The amount and localization of known RNP granule-related proteins were not disrupted in Fbxo24 KO mice, suggesting that the accumulated granules were distinct from known RNP granules. Further studies revealed that RNAs and two importins, IPO5 and KPNB1, abnormally accumulated in Fbxo24 KO spermatozoa and that FBXO24 could ubiquitinate IPO5. In addition, IPO5 and KPNB1 were recruited to stress granules, RNP complexes, when cells were treated with oxidative stress or a proteasome inhibitor. These results suggest that FBXO24 is involved in the degradation of IPO5, disruption of which may lead to the accumulation of abnormal RNP granules in sperm flagella.
