title: Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo.
abstract: Morphogenesis occurs in 3D space over time and is guided by coordinated gene expression programs. Here we use postembryonic development in Arabidopsis plants to investigate the genetic control of growth. We demonstrate that gene expression driving the production of the growth-stimulating hormone gibberellic acid and downstream growth factors is first induced within the radicle tip of the embryo. The center of cell expansion is, however, spatially displaced from the center of gene expression. Because the rapidly growing cells have very different geometry from that of those at the tip, we hypothesized that mechanical factors may contribute to this growth displacement. To this end we developed 3D finite-element method models of growing custom-designed digital embryos at cellular resolution. We used this framework to conceptualize how cell size, shape, and topology influence tissue growth and to explore the interplay of geometrical and genetic inputs into growth distribution. Our simulations showed that mechanical constraints are sufficient to explain the disconnect between the experimentally observed spatiotemporal patterns of gene expression and early postembryonic growth. The center of cell expansion is the position where genetic and mechanical facilitators of growth converge. We have thus uncovered a mechanism whereby 3D cellular geometry helps direct where genetically specified growth takes place.
authors.affiliation: School of Biosciences, University of Birmingham, Birmingham B15 2TT, United Kingdom; g.w.bassel@bham.ac.uk smith@mpipz.mpg.de.
authors.forename: George W
authors.initials: GW
authors.lastname: Bassel
authors.affiliation: School of Biosciences, University of Birmingham, Birmingham B15 2TT, United Kingdom;
authors.forename: Petra
authors.initials: P
authors.lastname: Stamm
authors.affiliation: Institute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland;
authors.forename: Gabriella
authors.initials: G
authors.lastname: Mosca
authors.affiliation: Institute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland;
authors.forename: Pierre
authors.initials: P
authors.lastname: Barbier de Reuille
authors.affiliation: School of Biosciences, University of Birmingham, Birmingham B15 2TT, United Kingdom;
authors.forename: Daniel J
authors.initials: DJ
authors.lastname: Gibbs
authors.affiliation: Division of Surgery, Department of Surgery and Cancer, Imperial College London, London W2 1NY, United Kingdom;
authors.forename: Robin
authors.initials: R
authors.lastname: Winter
authors.affiliation: Ecole d'Ingenieurs et d'Architectes de Fribourg, CH-1705 Fribourg, Switzerland;
authors.forename: Ales
authors.initials: A
authors.lastname: Janka
authors.affiliation: Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom; and.
authors.forename: Michael J
authors.initials: MJ
authors.lastname: Holdsworth
authors.affiliation: Institute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland;Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany g.w.bassel@bham.ac.uk smith@mpipz.mpg.de.
authors.forename: Richard S
authors.initials: RS
authors.lastname: Smith
mesh_terms: D000465:Algorithms; D017360:Arabidopsis / Q000196:embryology* / Q000235:genetics / Q000378:metabolism; D048430:Cell Shape; D048429:Cell Size; D018507:Gene Expression Regulation, Developmental; D018506:Gene Expression Regulation, Plant; D018525:Germination / Q000235:genetics; D005875:Gibberellins / Q000096:biosynthesis; D036341:Intercellular Signaling Peptides and Proteins / Q000096:biosynthesis; D018613:Microscopy, Confocal; D008954:Models, Biological; D030821:Plants, Genetically Modified; D012639:Seeds / Q000166:cytology* / Q000235:genetics / Q000254:growth & development; D013314:Stress, Mechanical
chemical_list: D005875:Gibberellins; D036341:Intercellular Signaling Peptides and Proteins; C007842:gibberellic acid
keywords: biomechanics; computational modeling; plant development; quantification; seed germination