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1.
Proc Natl Acad Sci U S A ; 120(6): e2214205120, 2023 02 07.
Article in English | MEDLINE | ID: mdl-36724258

ABSTRACT

Tissue flow during morphogenesis is commonly driven by local constriction of cell cortices, which is caused by the activation of actomyosin contractility. This can lead to long-range flows due to tissue viscosity. However, in the absence of cell-intrinsic polarized forces or polarity in forces external to the tissue, these flows must be symmetric and centered around the region of contraction. Polarized tissue flows have been previously demonstrated to arise from the coupling of such contractile flows to points of increased friction or adhesion to external structures. However, we show with experiments and modeling that the onset of polarized tissue flow in early Drosophila morphogenesis occurs independent of adhesion and is instead driven by a geometric coupling of apical actomyosin contractility to tissue curvature. Particularly, the onset of polarized flow is driven by a mismatch between the position of apical myosin activation and the position of peak curvature at the posterior pole of the embryo. Our work demonstrates how genetic and geometric information inherited from the mother interact to create polarized flow during embryo morphogenesis.


Subject(s)
Drosophila Proteins , Drosophila , Animals , Drosophila/genetics , Actomyosin/metabolism , Drosophila Proteins/metabolism , Myosins/metabolism , Morphogenesis/physiology , Drosophila melanogaster/metabolism , Embryo, Nonmammalian
2.
Curr Biol ; 28(19): 3031-3043.e2, 2018 10 08.
Article in English | MEDLINE | ID: mdl-30245102

ABSTRACT

Oriented cell divisions are significant in plant morphogenesis because plant cells are embedded in cell walls and cannot relocate. Cell divisions follow various regular orientations, but the underlying mechanisms have not been clarified. We propose that cell-shape-dependent self-organization of cortical microtubule arrays is able to provide a mechanism for determining planes of early tissue-generating divisions and may form the basis for robust control of cell division orientation in the embryo. To show this, we simulate microtubules on actual cell surface shapes, from which we derive a minimal set of three rules for proper array orientation. The first rule captures the effects of cell shape alone on microtubule organization, the second rule describes the regulation of microtubule stability at cell edges, and the third rule includes the differential effect of auxin on local microtubule stability. These rules generate early embryonic division plane orientations and potentially offer a framework for understanding patterned cell divisions in plant morphogenesis.


Subject(s)
Cell Division/physiology , Microtubules/physiology , Seeds/metabolism , Arabidopsis/metabolism , Arabidopsis Proteins/metabolism , Cell Shape/physiology , Computer Simulation , Embryonic Development , Indoleacetic Acids/metabolism , Meristem/metabolism , Orientation, Spatial , Plant Cells/physiology , Plant Development , Plant Roots/metabolism
3.
PLoS Comput Biol ; 14(2): e1005959, 2018 02.
Article in English | MEDLINE | ID: mdl-29394250

ABSTRACT

Plant morphogenesis is strongly dependent on the directional growth and the subsequent oriented division of individual cells. It has been shown that the plant cortical microtubule array plays a key role in controlling both these processes. This ordered structure emerges as the collective result of stochastic interactions between large numbers of dynamic microtubules. To elucidate this complex self-organization process a number of analytical and computational approaches to study the dynamics of cortical microtubules have been proposed. To date, however, these models have been restricted to two dimensional planes or geometrically simple surfaces in three dimensions, which strongly limits their applicability as plant cells display a wide variety of shapes. This limitation is even more acute, as both local as well as global geometrical features of cells are expected to influence the overall organization of the array. Here we describe a framework for efficiently simulating microtubule dynamics on triangulated approximations of arbitrary three dimensional surfaces. This allows the study of microtubule array organization on realistic cell surfaces obtained by segmentation of microscopic images. We validate the framework against expected or known results for the spherical and cubical geometry. We then use it to systematically study the individual contributions of global geometry, cell-edge induced catastrophes and cell-face induced stability to array organization in a cuboidal geometry. Finally, we apply our framework to analyze the highly non-trivial geometry of leaf pavement cells of Arabidopsis thaliana, Nicotiana benthamiana and Hedera helix. We show that our simulations can predict multiple features of the microtubule array structure in these cells, revealing, among others, strong constraints on the orientation of division planes.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/cytology , Computer Simulation , Microtubules/metabolism , Plant Cells , Software , Algorithms , Anisotropy , Cell Membrane/metabolism , Computational Biology , Hedera/cytology , Microscopy, Confocal , Models, Biological , Normal Distribution , Plant Leaves/cytology , Probability , Stochastic Processes , Nicotiana/cytology , Tubulin/metabolism
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