Organ geometry channels reproductive cell fate in the Arabidopsis ovule primordium.

Elvira Hernandez-Lagana,Arezki Boudaoud,Olivier Hamant,Daniel Grimanelli,Ethel Mendocilla-Sato,Ueli Grossniklaus,Daphné Autran,Christophe Godin,Alejandro Giraldo-Fonseca,Anja Frey,Gabriella Mosca,Caroline Michaud,Célia Baroux,Nuno Pires

doi:10.7554/elife.66031

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.

Highlights

A hallmark of sexual reproduction in multicellular organisms is the separation of the germline from the soma
The temporal resolution of our analysis led us to subdivide early stages covering primordium emergence prior to the straight digit-shape of the organ set as stage 1-I, where the spore mother cell (SMC) becomes distinguishable by its apparent larger size in longitudinal views (Grossniklaus and Schneitz, 1998; Figure 1B)
The female germline is initiated with SMC differentiation in the ovule primordium

Summary

Introduction

A hallmark of sexual reproduction in multicellular organisms is the separation of the germline from the soma. The number of germ cells depends on the balance between proliferation (selfrenewal) and differentiation, a process controlled by both intrinsic factors and signals from the surrounding somatic tissues. The first cells representing the germline, the spore mother cells (SMCs), differentiate only late in development. SMCs arise multiple times, in each flower during the formation of the reproductive organs. In Arabidopsis, the female SMC differentiates in the nucellus of the ovule primordium, a digit-shaped organ that emerges from the placental tissue of the gynoecium. The SMC is recognizable as a single, large, and elongated subepidermal cell, which is centrally positioned within the nucellus and displays a prominent nucleus and nucleolus (Bajon et al, 1999; Bowman, 1993; Schmidt et al, 2015; Schneitz et al, 1995)

Methods

Results

Conclusion