TY - JOUR
T1 - A computational framework for cortical microtubule dynamics in realistically shaped plant cells
AU - Chakrabortty, Bandan
AU - Blilou, Ikram
AU - Scheres, Ben
AU - Mulder, Bela M.
N1 - KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: The position of BC was funded by a grant of the Wageningen University IPOP Program. The majority of computations were made possible though computer time provided by the SURF Foundation GRID facility (contract no. 16079). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
PY - 2018/2/2
Y1 - 2018/2/2
N2 - 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.
AB - 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.
UR - http://hdl.handle.net/10754/627044
UR - http://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1005959
UR - http://www.scopus.com/inward/record.url?scp=85042697291&partnerID=8YFLogxK
U2 - 10.1371/journal.pcbi.1005959
DO - 10.1371/journal.pcbi.1005959
M3 - Article
C2 - 29394250
AN - SCOPUS:85042697291
VL - 14
SP - e1005959
JO - PLOS Computational Biology
JF - PLOS Computational Biology
SN - 1553-7358
IS - 2
ER -