Predicting Division Planes of Three-Dimensional Cells by Soap-Film Minimization

Pablo Martinez, Lindy A. Allsman, Kenneth A. Brakke, Christopher Hoyt, Jordan Hayes, Hong Liang, Wesley Neher, Yue Rui, Allyson M. Roberts, Amir Moradifam, Bob Goldstein, Charles T. Anderson, Carolyn G. Rasmussen

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

One key aspect of cell division in multicellular organisms is the orientation of the division plane. Proper division plane establishment contributes to normal plant body organization. To determine the importance of cell geometry in division plane orientation, we designed a three-dimensional probabilistic mathematical model to directly test the century-old hypothesis that cell divisions mimic soap-film minima. According to this hypothesis, daughter cells have equal volume and the division plane occurs where the surface area is at a minimum. We compared predicted division planes to a plant microtubule array that marks the division site, the preprophase band (PPB). PPB location typically matched one of the predicted divisions. Predicted divisions offset from the PPB occurred when a neighboring cell wall or PPB was directly adjacent to the predicted division site to avoid creating a potentially structurally unfavorable four-way junction. By comparing divisions of differently shaped plant cells (maize [Zea mays] epidermal cells and developing ligule cells and Arabidopsis thaliana guard cells) and animal cells (Caenorhabditis elegans embryonic cells) to divisions simulated in silico, we demonstrate the generality of this model to accurately predict in vivo division. This powerful model can be used to separate the contribution of geometry from mechanical stresses or developmental regulation in predicting division plane orientation.

Original languageEnglish (US)
Pages (from-to)2255-2266
Number of pages12
JournalThe Plant cell
Volume30
Issue number10
DOIs
StatePublished - Oct 1 2018

Fingerprint

Soaps
soaps
Cell Division
cells
Zea mays
cell division
Mechanical Stress
Caenorhabditis elegans
Plant Cells
probabilistic models
Statistical Models
mechanical stress
Arabidopsis
Microtubules
Computer Simulation
guard cells
Cell Wall
Theoretical Models
microtubules
surface area

All Science Journal Classification (ASJC) codes

  • Plant Science
  • Cell Biology

Cite this

Martinez, P., Allsman, L. A., Brakke, K. A., Hoyt, C., Hayes, J., Liang, H., ... Rasmussen, C. G. (2018). Predicting Division Planes of Three-Dimensional Cells by Soap-Film Minimization. The Plant cell, 30(10), 2255-2266. https://doi.org/10.1105/tpc.18.00401
Martinez, Pablo ; Allsman, Lindy A. ; Brakke, Kenneth A. ; Hoyt, Christopher ; Hayes, Jordan ; Liang, Hong ; Neher, Wesley ; Rui, Yue ; Roberts, Allyson M. ; Moradifam, Amir ; Goldstein, Bob ; Anderson, Charles T. ; Rasmussen, Carolyn G. / Predicting Division Planes of Three-Dimensional Cells by Soap-Film Minimization. In: The Plant cell. 2018 ; Vol. 30, No. 10. pp. 2255-2266.
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Martinez, P, Allsman, LA, Brakke, KA, Hoyt, C, Hayes, J, Liang, H, Neher, W, Rui, Y, Roberts, AM, Moradifam, A, Goldstein, B, Anderson, CT & Rasmussen, CG 2018, 'Predicting Division Planes of Three-Dimensional Cells by Soap-Film Minimization', The Plant cell, vol. 30, no. 10, pp. 2255-2266. https://doi.org/10.1105/tpc.18.00401

Predicting Division Planes of Three-Dimensional Cells by Soap-Film Minimization. / Martinez, Pablo; Allsman, Lindy A.; Brakke, Kenneth A.; Hoyt, Christopher; Hayes, Jordan; Liang, Hong; Neher, Wesley; Rui, Yue; Roberts, Allyson M.; Moradifam, Amir; Goldstein, Bob; Anderson, Charles T.; Rasmussen, Carolyn G.

In: The Plant cell, Vol. 30, No. 10, 01.10.2018, p. 2255-2266.

Research output: Contribution to journalArticle

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Martinez P, Allsman LA, Brakke KA, Hoyt C, Hayes J, Liang H et al. Predicting Division Planes of Three-Dimensional Cells by Soap-Film Minimization. The Plant cell. 2018 Oct 1;30(10):2255-2266. https://doi.org/10.1105/tpc.18.00401