A Plausible Microtubule-Based Mechanism for Cell Division Orientation in Plant Embryogenesis

Bandan Chakrabortty, Viola Willemsen, Thijs de Zeeuw, Che Yang Liao, Dolf Weijers, Bela Mulder*, Ben Scheres

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

14 Citations (Scopus)

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. Chakrabortty et al. show that a computational model for dynamic self-organization of cortical microtubules on experimentally extracted cell shapes provides a plausible molecular mechanism for division plane orientation in the first four divisions of early stage A. thaliana embryos, in WT as well as two developmental mutants bodenlos and clasp.

Original languageEnglish
Pages (from-to)3031-3043.e2
JournalCurrent Biology
Volume28
Issue number19
DOIs
Publication statusPublished - 8 Oct 2018

Fingerprint

Microtubules
Cell Division
microtubules
Embryonic Development
cell division
embryogenesis
Cell Shape
Cells
Plant Development
cells
embryo (plant)
morphogenesis
Embryonic Structures
Indoleacetic Acids
Robust control
Plant Cells
dynamic models
Cell Wall
auxins
Tissue

Keywords

  • arabidopsis
  • auxin
  • cell shape
  • computational modeling
  • cytokinesis
  • division orientation
  • embryogenesis
  • microtubules
  • systems biology

Cite this

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title = "A Plausible Microtubule-Based Mechanism for Cell Division Orientation in Plant Embryogenesis",
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. Chakrabortty et al. show that a computational model for dynamic self-organization of cortical microtubules on experimentally extracted cell shapes provides a plausible molecular mechanism for division plane orientation in the first four divisions of early stage A. thaliana embryos, in WT as well as two developmental mutants bodenlos and clasp.",
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author = "Bandan Chakrabortty and Viola Willemsen and {de Zeeuw}, Thijs and Liao, {Che Yang} and Dolf Weijers and Bela Mulder and Ben Scheres",
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language = "English",
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A Plausible Microtubule-Based Mechanism for Cell Division Orientation in Plant Embryogenesis. / Chakrabortty, Bandan; Willemsen, Viola; de Zeeuw, Thijs; Liao, Che Yang; Weijers, Dolf; Mulder, Bela; Scheres, Ben.

In: Current Biology, Vol. 28, No. 19, 08.10.2018, p. 3031-3043.e2.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - A Plausible Microtubule-Based Mechanism for Cell Division Orientation in Plant Embryogenesis

AU - Chakrabortty, Bandan

AU - Willemsen, Viola

AU - de Zeeuw, Thijs

AU - Liao, Che Yang

AU - Weijers, Dolf

AU - Mulder, Bela

AU - Scheres, Ben

PY - 2018/10/8

Y1 - 2018/10/8

N2 - 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. Chakrabortty et al. show that a computational model for dynamic self-organization of cortical microtubules on experimentally extracted cell shapes provides a plausible molecular mechanism for division plane orientation in the first four divisions of early stage A. thaliana embryos, in WT as well as two developmental mutants bodenlos and clasp.

AB - 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. Chakrabortty et al. show that a computational model for dynamic self-organization of cortical microtubules on experimentally extracted cell shapes provides a plausible molecular mechanism for division plane orientation in the first four divisions of early stage A. thaliana embryos, in WT as well as two developmental mutants bodenlos and clasp.

KW - arabidopsis

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KW - cell shape

KW - computational modeling

KW - cytokinesis

KW - division orientation

KW - embryogenesis

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