3D cellular morphometrics of ovule primordium development in Zea mays reveal differential division and growth dynamics specifying megaspore mother cell singleness

Inès Ouedraogo; Marc Lartaud; Célia Baroux; Gabriella Mosca; Luciana Delgado; Oliver Leblanc; Jean-Luc Verdeil; Geneviève Conéjéro; Daphné Autran

doi:10.3389/fpls.2023.1174171

3D cellular morphometrics of ovule primordium development in Zea mays reveal differential division and growth dynamics specifying megaspore mother cell singleness

Front Plant Sci. 2023 May 12:14:1174171. doi: 10.3389/fpls.2023.1174171. eCollection 2023.

Authors

Inès Ouedraogo¹, Marc Lartaud², Célia Baroux³, Gabriella Mosca³, Luciana Delgado⁴, Oliver Leblanc¹, Jean-Luc Verdeil², Geneviève Conéjéro⁵, Daphné Autran¹

Affiliations

¹ DIADE, University of Montpellier, IRD, CIRAD, Montpellier, France.
² AGAP, University of Montpellier, CIRAD, INRAE, Institut SupAgro, Montpellier, France.
³ Institute of Plant and Microbial Biology, Zürich-Basel Plant Science Center, University of Zürich, Zürich, Switzerland.
⁴ IICAR, CONICET, University of Rosario, Rosario, Argentina.
⁵ IPSIM, University of Montpellier, CNRS, INRAE, Institut SupAgro, Montpellier, France.

Abstract

Introduction: Differentiation of spore mother cells marks the somatic-to-reproductive transition in higher plants. Spore mother cells are critical for fitness because they differentiate into gametes, leading to fertilization and seed formation. The female spore mother cell is called the megaspore mother cell (MMC) and is specified in the ovule primordium. The number of MMCs varies by species and genetic background, but in most cases, only a single mature MMC enters meiosis to form the embryo sac. Multiple candidate MMC precursor cells have been identified in both rice and Arabidopsis, so variability in MMC number is likely due to conserved early morphogenetic events. In Arabidopsis, the restriction of a single MMC per ovule, or MMC singleness, is determined by ovule geometry. To look for potential conservation of MMC ontogeny and specification mechanisms, we undertook a morphogenetic description of ovule primordium growth at cellular resolution in the model crop maize.

Methods: We generated a collection of 48 three-dimensional (3D) ovule primordium images for five developmental stages, annotated for 11 cell types. Quantitative analysis of ovule and cell morphological descriptors allowed the reconstruction of a plausible developmental trajectory of the MMC and its neighbors.

Results: The MMC is specified within a niche of enlarged, homogenous L2 cells, forming a pool of candidate archesporial (MMC progenitor) cells. A prevalent periclinal division of the uppermost central archesporial cell formed the apical MMC and the underlying cell, a presumptive stack cell. The MMC stopped dividing and expanded, acquiring an anisotropic, trapezoidal shape. By contrast, periclinal divisions continued in L2 neighbor cells, resulting in a single central MMC.

Discussion: We propose a model where anisotropic ovule growth in maize drives L2 divisions and MMC elongation, coupling ovule geometry with MMC fate.

Keywords: 3D morphometrics; MMC specification; Zea mays; developmental atlas; female germ cell; morphogenesis; ovule primordium.

Grants and funding

This work was funded by a PRCI grant from the French Agence Nationale de la Recherche/Swiss National Science Foundation (IMAGO, #ANR-16-CE93-0002/SNF-310030L_170167) to DA and CB; an EU H2020 Marie Skłodowska-Curie Action Research and Innovation Staff Exchange grant (MAD, Grant agreement ID: 872417) to OL, DA, CB, and LD; a Labex AGRO-2011-LABX-002 (APOMOVIE, project number 1605-032), in the i-Site MUSE framework, coordinated by Agropolis Fondation grant to DA, GC, ML, and J-LV; and Agence Nationale de la Recherche (CHROMOBREED, #ANR-18-CE92-0041) and a PhD fellowship from U. Montpellier/French Ministère de la Recherche et de l’Enseignement Supérieur to IO.