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.

Highlights

  • In contrast to animal cells, plant cells are encased in a rigid cell wall providing among others the necessary rigidity to contain the turgor pressure that allows the plant as a whole to raise itself against gravity

  • It is well known that the cortical microtubule cytoskeleton in plant cells plays a decisive role in controlled cell expansion and oriented cell division, which together drive the plant morphogenesis [1]

  • To do so we considered the case of approximating a perfect sphere, varying both the number of triangles employed, as well as the triangulation method

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Summary

Introduction

It is well known that the cortical microtubule (hereafter abbreviated to MT) cytoskeleton in plant cells plays a decisive role in controlled cell expansion and oriented cell division, which together drive the plant morphogenesis [1]. The orientation of the CA controls cell expansion and cell anisotropy, by guiding the deposition of cellulose synthase complexes along the MTs [5,6,7,8]. Through this coupling, the CA in turn can influence the cell shape, essentially setting up a morphogenetic feedback loop. The CA in turn can influence the cell shape, essentially setting up a morphogenetic feedback loop This loop is possibly amplified by a mechanical feedback mechanism discussed in [9]. Understanding both anisotropic cell expansion and oriented cell division, requires understanding the formation of the ordered CA from an initially disordered state just after cell division [10]

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