A computational framework for cortical microtubule dynamics in realistically shaped plant cells

Handle URI:
http://hdl.handle.net/10754/627044
Title:
A computational framework for cortical microtubule dynamics in realistically shaped plant cells
Authors:
Chakrabortty, Bandan ( 0000-0002-4797-5732 ) ; Blilou, Ikram; Scheres, Ben; Mulder, Bela M. ( 0000-0002-8620-5749 )
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.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Plant Science Program; Desert Agriculture Initiative; Laboratory of plant cell and developmental biology, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia.
Citation:
Chakrabortty B, Blilou I, Scheres B, Mulder BM (2018) A computational framework for cortical microtubule dynamics in realistically shaped plant cells. PLOS Computational Biology 14: e1005959. Available: http://dx.doi.org/10.1371/journal.pcbi.1005959.
Publisher:
Public Library of Science (PLoS)
Journal:
PLOS Computational Biology
Issue Date:
2-Feb-2018
DOI:
10.1371/journal.pcbi.1005959
Type:
Article
ISSN:
1553-7358
Sponsors:
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.
Additional Links:
http://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1005959
Appears in Collections:
Articles; Plant Science Program; Desert Agriculture Initiative; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorChakrabortty, Bandanen
dc.contributor.authorBlilou, Ikramen
dc.contributor.authorScheres, Benen
dc.contributor.authorMulder, Bela M.en
dc.date.accessioned2018-02-07T07:02:23Z-
dc.date.available2018-02-07T07:02:23Z-
dc.date.issued2018-02-02en
dc.identifier.citationChakrabortty B, Blilou I, Scheres B, Mulder BM (2018) A computational framework for cortical microtubule dynamics in realistically shaped plant cells. PLOS Computational Biology 14: e1005959. Available: http://dx.doi.org/10.1371/journal.pcbi.1005959.en
dc.identifier.issn1553-7358en
dc.identifier.doi10.1371/journal.pcbi.1005959en
dc.identifier.urihttp://hdl.handle.net/10754/627044-
dc.description.abstractPlant 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.en
dc.description.sponsorshipThe 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.en
dc.publisherPublic Library of Science (PLoS)en
dc.relation.urlhttp://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1005959en
dc.rightsThis 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.en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleA computational framework for cortical microtubule dynamics in realistically shaped plant cellsen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentPlant Science Programen
dc.contributor.departmentDesert Agriculture Initiativeen
dc.contributor.departmentLaboratory of plant cell and developmental biology, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia.en
dc.identifier.journalPLOS Computational Biologyen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionPlant Developmental Biology, Wageningen University, Wageningen, The Netherlands.en
dc.contributor.institutionDepartment of Living Matter, Institute AMOLF, Amsterdam, The Netherlands.en
kaust.authorBlilou, Ikramen
All Items in KAUST are protected by copyright, with all rights reserved, unless otherwise indicated.