Analysis of cell division patterns in the Arabidopsis shoot apical meristem
Abstract
The stereotypic pattern of cell shapes in the Arabidopsis shoot apical meristem (SAM) suggests that strict rules govern the placement of new walls during cell division. When a cell in the SAM divides, a new wall is built that connects existing walls and divides the cytoplasm of the daughter cells. Because features that are determined by the placement of new walls such as cell size, shape, and number of neighbors are highly regular, rules must exist for maintaining such order. Here in this paper we present a quantitative model of these rules that incorporates different observed features of cell division. Each feature is incorporated into a "potential function" that contributes a single term to a total analog of potential energy. New cell walls are predicted to occur at locations where the potential function is minimized. Quantitative terms that represent the well-known historical rules of plant cell division, such as those given by Hofmeister, Errera, and Sachs are developed and evaluated against observed cell divisions in the epidermal layer (L1) of Arabidopsis thaliana SAM. The method is general enough to allow additional terms for nongeometric properties such as internal concentration gradients and mechanical tensile forces.
- Authors:
-
- Department of Mathematics, California State University, Northridge, CA 91330,, Division of Biology and Biological Engineering and
- Division of Biology and Biological Engineering and
- Department of Computer Science, University of California, Irvine, CA 92697
- Division of Biology and Biological Engineering and, Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125, and
- Publication Date:
- Research Org.:
- California Institute of Technology (CalTech), Pasadena, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1235160
- Alternate Identifier(s):
- OSTI ID: 1349045
- Grant/Contract Number:
- FG02-88ER13873; R01-GM086883; P50GM76516
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 112 Journal Issue: 15; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Arabidopsis; cell division; computer modeling; live imaging
Citation Formats
Shapiro, Bruce E., Tobin, Cory, Mjolsness, Eric, and Meyerowitz, Elliot M. Analysis of cell division patterns in the Arabidopsis shoot apical meristem. United States: N. p., 2015.
Web. doi:10.1073/pnas.1502588112.
Shapiro, Bruce E., Tobin, Cory, Mjolsness, Eric, & Meyerowitz, Elliot M. Analysis of cell division patterns in the Arabidopsis shoot apical meristem. United States. https://doi.org/10.1073/pnas.1502588112
Shapiro, Bruce E., Tobin, Cory, Mjolsness, Eric, and Meyerowitz, Elliot M. Mon .
"Analysis of cell division patterns in the Arabidopsis shoot apical meristem". United States. https://doi.org/10.1073/pnas.1502588112.
@article{osti_1235160,
title = {Analysis of cell division patterns in the Arabidopsis shoot apical meristem},
author = {Shapiro, Bruce E. and Tobin, Cory and Mjolsness, Eric and Meyerowitz, Elliot M.},
abstractNote = {The stereotypic pattern of cell shapes in the Arabidopsis shoot apical meristem (SAM) suggests that strict rules govern the placement of new walls during cell division. When a cell in the SAM divides, a new wall is built that connects existing walls and divides the cytoplasm of the daughter cells. Because features that are determined by the placement of new walls such as cell size, shape, and number of neighbors are highly regular, rules must exist for maintaining such order. Here in this paper we present a quantitative model of these rules that incorporates different observed features of cell division. Each feature is incorporated into a "potential function" that contributes a single term to a total analog of potential energy. New cell walls are predicted to occur at locations where the potential function is minimized. Quantitative terms that represent the well-known historical rules of plant cell division, such as those given by Hofmeister, Errera, and Sachs are developed and evaluated against observed cell divisions in the epidermal layer (L1) of Arabidopsis thaliana SAM. The method is general enough to allow additional terms for nongeometric properties such as internal concentration gradients and mechanical tensile forces.},
doi = {10.1073/pnas.1502588112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 15,
volume = 112,
place = {United States},
year = {Mon Mar 30 00:00:00 EDT 2015},
month = {Mon Mar 30 00:00:00 EDT 2015}
}
https://doi.org/10.1073/pnas.1502588112
Web of Science
Works referenced in this record:
A Modeling Study on How Cell Division Affects Properties of Epithelial Tissues Under Isotropic Growth
journal, July 2010
- Sahlin, Patrik; Jönsson, Henrik
- PLoS ONE, Vol. 5, Issue 7
The initial protrusion of a leaf primordium can form without concurrent periclinal cell divisions
journal, September 1971
- Foard, Donald E.
- Canadian Journal of Botany, Vol. 49, Issue 9
Regulatory Role of Cell Division Rules on Tissue Growth Heterogeneity
journal, August 2012
- Alim, Karen; Hamant, Olivier; Boudaoud, Arezki
- Frontiers in Plant Science, Vol. 3
Mechanical Signals in Plant Development: A New Method for Single Cell Studies
journal, January 1997
- Lynch, Timothy M.; Lintilhac, Philip M.
- Developmental Biology, Vol. 181, Issue 2
The Relative Position of cell Walls in Developing Plant Tissues
journal, July 1941
- Sinnott, Edmund W.; Bloch, Robert
- American Journal of Botany, Vol. 28, Issue 7
Plant cell division: building walls in the right places
journal, January 2001
- Smith, Laurie G.
- Nature Reviews Molecular Cell Biology, Vol. 2, Issue 1
Energy-Minimization Approach to the Atomic Geometry of Semiconductor Surfaces
journal, October 1978
- Chadi, D. J.
- Physical Review Letters, Vol. 41, Issue 15
Elastic Domains Regulate Growth and Organogenesis in the Plant Shoot Apical Meristem
journal, March 2012
- Kierzkowski, D.; Nakayama, N.; Routier-Kierzkowska, A. -L.
- Science, Vol. 335, Issue 6072
The Relationship Between the Distribution of Periclinal Cell Divisions in the Shoot Apex and Leaf Initiation
journal, June 1986
- Cunninghame, M. E.; Lyndon, R. F.
- Annals of Botany, Vol. 57, Issue 6
The Initiation and Determination of Leaves
journal, September 1992
- Smith, Laurie G.; Hake, Sarah
- The Plant Cell, Vol. 4, Issue 9
Nucleus-associated microtubules help determine the division plane of plant epidermal cells: avoidance of four-way junctions and the role of cell geometry
journal, April 1990
- Flanders, D. J.
- The Journal of Cell Biology, Vol. 110, Issue 4
Demonstration of the Three germ Layers in the Shoot apex of Datura by Means of Induced Polyploidy in Periclinal Chimeras
journal, December 1940
- Satina, S.; Blakeslee, A. F.; Avery, Amos G.
- American Journal of Botany, Vol. 27, Issue 10
Cell fate in the shoot apical meristem of Arabidopsis thaliana
journal, July 1992
- Furner I., J.; Pumfrey, J. E.
- Development, Vol. 115, Issue 3
Imaging plant growth in 4D: robust tissue reconstruction and lineaging at cell resolution
journal, June 2010
- Fernandez, Romain; Das, Pradeep; Mirabet, Vincent
- Nature Methods, Vol. 7, Issue 7
Stem-Cell Homeostasis and Growth Dynamics Can Be Uncoupled in the Arabidopsis Shoot Apex
journal, October 2005
- Reddy, G. V.
- Science, Vol. 310, Issue 5748
The shoot apical meristem: the dynamics of a stable structure
journal, June 2002
- Traas, Jan; Vernoux, Teva
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 357, Issue 1422
Universal rule for the symmetric division of plant cells
journal, March 2011
- Besson, S.; Dumais, J.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 15
Structural integration at the shoot apical meristem: models, measurements, and experiments
journal, September 2004
- Kwiatkowska, D.
- American Journal of Botany, Vol. 91, Issue 9
The Preprophase Band of Microtubules: Its Function as a Cytokinetic Apparatus in Higher Plants
book, January 1999
- Mineyuki, Yoshinobu
- International Review of Cytology