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      Cell geometry determines symmetric and asymmetric division plane selection in Arabidopsis early embryos

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          Abstract

          Plant tissue architecture and organ morphogenesis rely on the proper orientation of cell divisions. Previous attempts to predict division planes from cell geometry in plants mostly focused on 2D symmetric divisions. Using the stereotyped division patterns of Arabidopsis thaliana early embryogenesis, we investigated geometrical principles underlying plane selection in symmetric and in asymmetric divisions within complex 3D cell shapes. Introducing a 3D computational model of cell division, we show that area minimization constrained on passing through the cell centroid predicts observed divisions. Our results suggest that the positioning of division planes ensues from cell geometry and gives rise to spatially organized cell types with stereotyped shapes, thus underlining the role of self-organization in the developing architecture of the embryo. Our data further suggested the rule could be interpreted as surface minimization constrained by the nucleus position, which was validated using live imaging of cell divisions in the stomatal cell lineage.

          Author summary

          The proper positioning of division planes is key for correct development and morphogenesis of organs, in particular in plants were cellular walls prevent cell rearrangements. Elucidating how division planes are selected is therefore essential to decipher the cellular bases of plant morphogenesis. Previous attempts to identify geometrical rules relating cell shape and division plane positioning in plants mostly focused on symmetric divisions in tissues reduced to 2D geometries. Here, we combined 3D quantitative image analysis and a new 3D cell division model to evaluate the existence of geometrical rules in asymmetrical and symmetrical divisions of complex cell shapes. We show that in the early embryo of the model plant Arabidopsis thaliana, which presents stereotyped but complex cell division patterns, a single geometrical rule (area minimization constrained on passing through the cell centroid) recapitulates the complete sequence of division events. This new rule, valid for both symmetrical and asymmetrical divisions, generalizes previously proposed cell division rules and can be interpreted based on the dynamics of the cytoskeleton and on the positioning of the nucleus, a hypothesis that we validated using leaf cell division patterns. This work highlights the importance of self-organization in plant early morphogenesis and the emergence of robust cellular organizations based on geometrical feedback loops between cell geometry and division plane selection.

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          Most cited references50

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          An unbiased detector of curvilinear structures

          J Steger (1998)
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            High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis.

            Currently, examination of the cellular structure of plant organs and the gene expression therein largely relies on the production of tissue sections. Here, we present a staining technique that can be used to image entire plant organs using confocal laser scanning microscopy. This technique produces high-resolution images that allow three-dimensional reconstruction of the cellular organization of plant organs. Importantly, three-dimensional domains of gene expression can be analyzed with single-cell precision. We used this technique for a detailed examination of phloem cells in the wild type and mutants. We were also able to recognize phloem sieve elements and their differentiation state in any tissue type and visualize the structure of sieve plates. We show that in the altered phloem development mutant, a hybrid cell type with phloem and xylem characteristics develops from initially normally differentiated protophloem cells. The simplicity of sieve element data collection allows for the statistical analysis of structural parameters of sieve plates, essential for the calculation of phloem conductivity. Taken together, this technique significantly improves the speed and accuracy of the investigation of plant growth and development.
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              Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis.

              In plants, the developmental mechanisms that regulate the positioning of lateral organs along the primary root are currently unknown. We present evidence on how lateral root initiation is controlled in a spatiotemporal manner in the model plant Arabidopsis thaliana. First, lateral roots are spaced along the main axis in a regular left-right alternating pattern that correlates with gravity-induced waving and depends on AUX1, an auxin influx carrier essential for gravitropic response. Second, we found evidence that the priming of pericycle cells for lateral root initiation might take place in the basal meristem, correlating with elevated auxin sensitivity in this part of the root. This local auxin responsiveness oscillates with peaks of expression at regular intervals of 15 hours. Each peak in the auxin-reporter maximum correlates with the formation of a consecutive lateral root. Third, auxin signaling in the basal meristem triggers pericycle cells for lateral root initiation prior to the action of INDOLE-3-ACETIC ACID14 (SOLITARY ROOT).
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Visualization
                Role: Formal analysisRole: InvestigationRole: Software
                Role: Investigation
                Role: Formal analysisRole: Investigation
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                February 2019
                11 February 2019
                : 15
                : 2
                : e1006771
                Affiliations
                [1 ] Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, 78000 Versailles, France
                [2 ] MaIAGE, INRA, Université Paris-Saclay, 78350, Jouy-en-Josas, France
                [3 ] INRA, UMR782 Génie et Microbiologie des Procédés Alimentaires, 78850 Thiverval-Grignon, France
                Oxford, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                [¤a]

                Current address: Laboratoire Matière et Systèmes Complexes, CNRS, Université Denis Diderot, 75013 Paris, France

                [¤b]

                Current address: Unité Biopolymères Interactions Assemblages, INRA, 44000 Nantes, France

                [¤c]

                Current address: Institut d’Optique Graduate School, Laboratoire Charles Fabry, 91127 Palaiseau, France

                [¤d]

                Current address: Alstom Transport, St-Ouen, France

                Author information
                http://orcid.org/0000-0002-7861-0437
                http://orcid.org/0000-0001-5932-6863
                Article
                PCOMPBIOL-D-18-00460
                10.1371/journal.pcbi.1006771
                6386405
                30742612
                649473d2-4bd7-44dd-8954-e8eb291bb93f
                © 2019 Moukhtar et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 March 2018
                : 10 January 2019
                Page count
                Figures: 6, Tables: 0, Pages: 27
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-10-LABX-0040-SPS
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100006488, Institut National de la Recherche Agronomique;
                Award Recipient :
                This work has benefited from a French State grant (ANR-10-LABX-0040-SPS) managed by the French National Research Agency under the Investments for the Future program (ANR-11-IDEX-0003-02). AU was funded by an INRA fellowship. JM was funded by the Saclay Plant Sciences LabEx. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cell Cycle and Cell Division
                Biology and Life Sciences
                Developmental Biology
                Embryology
                Embryos
                Research and Analysis Methods
                Bioassays and Physiological Analysis
                Cell Analysis
                Cell Division Analysis
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Model Organisms
                Arabidopsis Thaliana
                Research and Analysis Methods
                Model Organisms
                Arabidopsis Thaliana
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Brassica
                Arabidopsis Thaliana
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Plant and Algal Models
                Arabidopsis Thaliana
                Research and Analysis Methods
                Simulation and Modeling
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Plant Cells
                Biology and Life Sciences
                Cell Biology
                Plant Cell Biology
                Plant Cells
                Biology and Life Sciences
                Plant Science
                Plant Cell Biology
                Plant Cells
                Biology and Life Sciences
                Developmental Biology
                Morphogenesis
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-02-22
                All relevant data are within the paper and its Supporting Information files. The C++ code of the model and an executable version (Linux Ubuntu 16.04 64-bits) can be found at http://www-ijpb.versailles.inra.fr/en/bc/equipes/modelisation-imagerie/.

                Quantitative & Systems biology
                Quantitative & Systems biology

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