Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells
Abstract
Although it is a central question in biology, how cell shape controls intracellular dynamics largely remains an open question. Here, we show that the shape of Arabidopsis pavement cells creates a stress pattern that controls microtubule orientation, which then guides cell wall reinforcement. Live-imaging, combined with modeling of cell mechanics, shows that microtubules align along the maximal tensile stress direction within the cells, and atomic force microscopy demonstrates that this leads to reinforcement of the cell wall parallel to the microtubules. This feedback loop is regulated: cell-shape derived stresses could be overridden by imposed tissue level stresses, showing how competition between subcellular and supracellular cues control microtubule behavior. Furthermore, at the microtubule level, we identified an amplification mechanism in which mechanical stress promotes the microtubule response to stress by increasing severing activity. These multiscale feedbacks likely contribute to the robustness of microtubule behavior in plant epidermis.
- Authors:
- Publication Date:
- Research Org.:
- California Institute of Technology (CalTech), Pasadena, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1197663
- Alternate Identifier(s):
- OSTI ID: 1197668; OSTI ID: 1628807
- Grant/Contract Number:
- FG02-88ER13873
- Resource Type:
- Published Article
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Name: eLife Journal Volume: 3; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Life Sciences & Biomedicine - Other Topics
Citation Formats
Sampathkumar, Arun, Krupinski, Pawel, Wightman, Raymond, Milani, Pascale, Berquand, Alexandre, Boudaoud, Arezki, Hamant, Olivier, Jönsson, Henrik, and Meyerowitz, Elliot M. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. United States: N. p., 2014.
Web. doi:10.7554/eLife.01967.
Sampathkumar, Arun, Krupinski, Pawel, Wightman, Raymond, Milani, Pascale, Berquand, Alexandre, Boudaoud, Arezki, Hamant, Olivier, Jönsson, Henrik, & Meyerowitz, Elliot M. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. United States. https://doi.org/10.7554/eLife.01967
Sampathkumar, Arun, Krupinski, Pawel, Wightman, Raymond, Milani, Pascale, Berquand, Alexandre, Boudaoud, Arezki, Hamant, Olivier, Jönsson, Henrik, and Meyerowitz, Elliot M. Wed .
"Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells". United States. https://doi.org/10.7554/eLife.01967.
@article{osti_1197663,
title = {Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells},
author = {Sampathkumar, Arun and Krupinski, Pawel and Wightman, Raymond and Milani, Pascale and Berquand, Alexandre and Boudaoud, Arezki and Hamant, Olivier and Jönsson, Henrik and Meyerowitz, Elliot M.},
abstractNote = {Although it is a central question in biology, how cell shape controls intracellular dynamics largely remains an open question. Here, we show that the shape of Arabidopsis pavement cells creates a stress pattern that controls microtubule orientation, which then guides cell wall reinforcement. Live-imaging, combined with modeling of cell mechanics, shows that microtubules align along the maximal tensile stress direction within the cells, and atomic force microscopy demonstrates that this leads to reinforcement of the cell wall parallel to the microtubules. This feedback loop is regulated: cell-shape derived stresses could be overridden by imposed tissue level stresses, showing how competition between subcellular and supracellular cues control microtubule behavior. Furthermore, at the microtubule level, we identified an amplification mechanism in which mechanical stress promotes the microtubule response to stress by increasing severing activity. These multiscale feedbacks likely contribute to the robustness of microtubule behavior in plant epidermis.},
doi = {10.7554/eLife.01967},
journal = {eLife},
number = ,
volume = 3,
place = {United States},
year = {Wed Apr 16 00:00:00 EDT 2014},
month = {Wed Apr 16 00:00:00 EDT 2014}
}
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Works referenced in this record:
A Mechanism for Reorientation of Cortical Microtubule Arrays Driven by Microtubule Severing
journal, November 2013
- Lindeboom, J. J.; Nakamura, M.; Hibbel, A.
- Science, Vol. 342, Issue 6163
Pulsed Forces Timed by a Ratchet-like Mechanism Drive Directed Tissue Movement during Dorsal Closure
journal, June 2009
- Solon, Jerome; Kaya-Çopur, Aynur; Colombelli, Julien
- Cell, Vol. 137, Issue 7
Experimental and theoretical study of mitotic spindle orientation
journal, May 2007
- Théry, Manuel; Jiménez-Dalmaroni, Andrea; Racine, Victor
- Nature, Vol. 447, Issue 7143
Organogenesis-A Biophysical View
journal, June 1980
- Green, P. B.
- Annual Review of Plant Physiology, Vol. 31, Issue 1
The epidermal-growth-control theory of stem elongation: An old and a new perspective
journal, November 2007
- Kutschera, U.; Niklas, K. J.
- Journal of Plant Physiology, Vol. 164, Issue 11
The growth speed of microtubules with XMAP215-coated beads coupled to their ends is increased by tensile force
journal, August 2013
- Trushko, Anastasiya; Schäffer, Erik; Howard, Jonathon
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 36
Mechanical feedback as a possible regulator of tissue growth
journal, February 2005
- Shraiman, B. I.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 9
Effect of contact deformations on the adhesion of particles
journal, November 1975
- Derjaguin, B. V.; Muller, V. M.; Toporov, Yu. P.
- Journal of Colloid and Interface Science, Vol. 53, Issue 2
Calibration of atomic‐force microscope tips
journal, July 1993
- Hutter, Jeffrey L.; Bechhoefer, John
- Review of Scientific Instruments, Vol. 64, Issue 7
Cell Polarity Signaling in Arabidopsis
journal, November 2008
- Yang, Zhenbiao
- Annual Review of Cell and Developmental Biology, Vol. 24, Issue 1
Variability in the Control of Cell Division Underlies Sepal Epidermal Patterning in Arabidopsis thaliana
journal, May 2010
- Roeder, Adrienne H. K.; Chickarmane, Vijay; Cunha, Alexandre
- PLoS Biology, Vol. 8, Issue 5
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 Importance of Lattice Defects in Katanin-Mediated Microtubule Severing in Vitro
journal, June 2002
- Davis, Liza J.; Odde, David J.; Block, Steven M.
- Biophysical Journal, Vol. 82, Issue 6
Tension applied through the Dam1 complex promotes microtubule elongation providing a direct mechanism for length control in mitosis
journal, June 2007
- Franck, Andrew D.; Powers, Andrew F.; Gestaut, Daniel R.
- Nature Cell Biology, Vol. 9, Issue 7
Cell shaping and microtubules in developing mesophyll of wheat (Triticum aestivum L.)
journal, October 1990
- Jung, G.; Wernicke, W.
- Protoplasma, Vol. 153, Issue 3
Cell cycle regulates cell type in the Arabidopsis sepal
journal, October 2012
- Roeder, A. H. K.; Cunha, A.; Ohno, C. K.
- Development, Vol. 139, Issue 23
Cell Surface- and Rho GTPase-Based Auxin Signaling Controls Cellular Interdigitation in Arabidopsis
journal, October 2010
- Xu, Tongda; Wen, Mingzhang; Nagawa, Shingo
- Cell, Vol. 143, Issue 1
The Forces that Move Chromosomes in Mitosis
journal, June 1988
- Nicklas, R. B.
- Annual Review of Biophysics and Biophysical Chemistry, Vol. 17, Issue 1
POM-POM2/CELLULOSE SYNTHASE INTERACTING1 Is Essential for the Functional Association of Cellulose Synthase and Microtubules in Arabidopsis
journal, January 2012
- Bringmann, Martin; Li, Eryang; Sampathkumar, Arun
- The Plant Cell, Vol. 24, Issue 1
Biomechanics of plant growth
journal, October 2006
- Schopfer, P.
- American Journal of Botany, Vol. 93, Issue 10
The rotation of cellulose synthase trajectories is microtubule dependent and influences the texture of epidermal cell walls in Arabidopsis hypocotyls
journal, September 2010
- Chan, J.; Crowell, E.; Eder, M.
- Journal of Cell Science, Vol. 123, Issue 20
Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells: a push-pull mechanism
journal, August 1993
- Skibbens, R. V.
- The Journal of Cell Biology, Vol. 122, Issue 4
SPIRAL2 Determines Plant Microtubule Organization by Modulating Microtubule Severing
journal, October 2013
- Wightman, Raymond; Chomicki, Guillaume; Kumar, Manoj
- Current Biology, Vol. 23, Issue 19
Viscoelastic properties of cell walls of single living plant cells determined by dynamic nanoindentation
journal, January 2012
- Hayot, Céline M.; Forouzesh, Elham; Goel, Ashwani
- Journal of Experimental Botany, Vol. 63, Issue 7
Differential Regulation of Cellulose Orientation at the Inner and Outer Face of Epidermal Cells in the Arabidopsis Hypocotyl
journal, July 2011
- Crowell, Elizabeth Faris; Timpano, Hélène; Desprez, Thierry
- The Plant Cell, Vol. 23, Issue 7
Microtubule Severing at Crossover Sites by Katanin Generates Ordered Cortical Microtubule Arrays in Arabidopsis
journal, November 2013
- Zhang, Quan; Fishel, Erica; Bertroche, Tyler
- Current Biology, Vol. 23, Issue 21
Alignment between PIN1 Polarity and Microtubule Orientation in the Shoot Apical Meristem Reveals a Tight Coupling between Morphogenesis and Auxin Transport
journal, October 2010
- Heisler, Marcus G.; Hamant, Olivier; Krupinski, Pawel
- PLoS Biology, Vol. 8, Issue 10
The Relationship of Cells to Organisms in Plants: Problem and Implications of an Organismal Perspective
journal, September 1992
- Kaplan, Donald R.
- International Journal of Plant Sciences, Vol. 153, Issue 3, Part 2
Arabidopsis Interdigitating Cell Growth Requires Two Antagonistic Pathways with Opposing Action on Cell Morphogenesis
journal, March 2005
- Fu, Ying; Gu, Ying; Zheng, Zhiliang
- Cell, Vol. 120, Issue 5
BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis
journal, January 2001
- Bichet, Adeline; Desnos, Thierry; Turner, Simon
- The Plant Journal, Vol. 25, Issue 2
The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile
journal, May 1965
- Sneddon, Ian N.
- International Journal of Engineering Science, Vol. 3, Issue 1
Mechanical Stress Acts via Katanin to Amplify Differences in Growth Rate between Adjacent Cells in Arabidopsis
journal, April 2012
- Uyttewaal, Magalie; Burian, Agata; Alim, Karen
- Cell, Vol. 149, Issue 2
Onion epidermis as a new model to study the control of growth anisotropy in higher plants
journal, August 2009
- Suslov, D.; Verbelen, J. -P.; Vissenberg, K.
- Journal of Experimental Botany, Vol. 60, Issue 14
The mechanics behind cell polarity
journal, November 2012
- Asnacios, Atef; Hamant, Olivier
- Trends in Cell Biology, Vol. 22, Issue 11
Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules
journal, June 2006
- Paredez, A. R.
- Science, Vol. 312, Issue 5779
Matrix Elasticity Directs Stem Cell Lineage Specification
journal, August 2006
- Engler, Adam J.; Sen, Shamik; Sweeney, H. Lee
- Cell, Vol. 126, Issue 4, p. 677-689
Regulation of Growth Anisotropy in Well-Watered and Water-Stressed Maize Roots. II. Role of Cortical Microtubules and Cellulose Microfibrils
journal, February 1999
- Baskin, Tobias I.; Meekes, Herman T. H. M.; Liang, Benjamin M.
- Plant Physiology, Vol. 119, Issue 2
Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays: Microtubule dynamics
journal, September 2007
- Wightman, Raymond; Turner, Simon R.
- The Plant Journal, Vol. 52, Issue 4
Regulative feedback in pattern formation: towards a general relativistic theory of positional information
journal, August 2008
- Jaeger, J.; Irons, D.; Monk, N.
- Development, Vol. 135, Issue 19
In vivo analysis of local wall stiffness at the shoot apical meristem in Arabidopsis using atomic force microscopy: Measuring wall stiffness in meristems with AFM
journal, July 2011
- Milani, Pascale; Gholamirad, Maryam; Traas, Jan
- The Plant Journal, Vol. 67, Issue 6
Rho GTPase Signaling Activates Microtubule Severing to Promote Microtubule Ordering in Arabidopsis
journal, February 2013
- Lin, Deshu; Cao, Lingyan; Zhou, Zhenzhen
- Current Biology, Vol. 23, Issue 4
Morphogen Gradient Formation
journal, July 2009
- Wartlick, O.; Kicheva, A.; Gonzalez-Gaitan, M.
- Cold Spring Harbor Perspectives in Biology, Vol. 1, Issue 3
An auxin-driven polarized transport model for phyllotaxis
journal, January 2006
- Jonsson, H.; Heisler, M. G.; Shapiro, B. E.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 5
The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells
journal, January 2011
- Zhang, Chunhua; Halsey, Leah E.; Szymanski, Daniel B.
- BMC Plant Biology, Vol. 11, Issue 1
Tension-dependent Regulation of Microtubule Dynamics at Kinetochores Can Explain Metaphase Congression in Yeast
journal, August 2005
- Gardner, Melissa K.; Pearson, Chad G.; Sprague, Brian L.
- Molecular Biology of the Cell, Vol. 16, Issue 8
New Evidence for the Role of Mechanical Forces in the Shoot Apical Meristem
journal, March 2000
- Dumais, Jacques; Steele, Charles R.
- Journal of Plant Growth Regulation, Vol. 19, Issue 1
Finite element implementation of incompressible, transversely isotropic hyperelasticity
journal, August 1996
- Weiss, Jeffrey A.; Maker, Bradley N.; Govindjee, Sanjay
- Computer Methods in Applied Mechanics and Engineering, Vol. 135, Issue 1-2
Mechanical properties of primary plant cell wall analogues
journal, October 2002
- Chanliaud, Elisabeth; Burrows, Kathleen; Jeronimidis, George
- Planta, Vol. 215, Issue 6
Measuring the spring constant of atomic force microscope cantilevers: thermal fluctuations and other methods
journal, December 2001
- Lévy, R.; Maaloum, M.
- Nanotechnology, Vol. 13, Issue 1
Alignment of Cortical Microtubules by Anisotropic Wall Stresses
journal, January 1990
- Williamson, Re
- Functional Plant Biology, Vol. 17, Issue 6
Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis: Microtubules and cell-wall crystallinity
journal, April 2011
- Fujita, Miki; Himmelspach, Regina; Hocart, Charles H.
- The Plant Journal, Vol. 66, Issue 6
Positional information and the spatial pattern of cellular differentiation
journal, October 1969
- Wolpert, L.
- Journal of Theoretical Biology, Vol. 25, Issue 1
Mechanical Signals Trigger Myosin II Redistribution and Mesoderm Invagination in Drosophila Embryos
journal, April 2009
- Pouille, P. -A.; Ahmadi, P.; Brunet, A. -C.
- Science Signaling, Vol. 2, Issue 66
Mechanical stress in Arabidopsis leaves orients microtubules in a 'continuous’ supracellular pattern
journal, January 2013
- Jacques, Eveline; Verbelen, Jean-Pierre; Vissenberg, Kris
- BMC Plant Biology, Vol. 13, Issue 1
FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images
journal, January 2014
- Boudaoud, Arezki; Burian, Agata; Borowska-Wykręt, Dorota
- Nature Protocols, Vol. 9, Issue 2
Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors
journal, August 2012
- Stylianopoulos, T.; Martin, J. D.; Chauhan, V. P.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 38
Eukaryotic Cells and their Cell Bodies: Cell Theory Revised
journal, May 2004
- BALUsKA, F.
- Annals of Botany, Vol. 94, Issue 1
Drosophila Katanin-60 Depolymerizes and Severs at Microtubule Defects
journal, May 2011
- Díaz-Valencia, Juan Daniel; Morelli, Margaret M.; Bailey, Megan
- Biophysical Journal, Vol. 100, Issue 10
Quantification of the Young's modulus of the primary plant cell wall using Bending-Lab-On-Chip (BLOC)
journal, January 2013
- Nezhad, Amir Sanati; Naghavi, Mahsa; Packirisamy, Muthukumaran
- Lab on a Chip, Vol. 13, Issue 13
The Role of Microtubules in Guard Cell Function
journal, January 2001
- Marcus, Adam I.; Moore, Richard C.; Cyr, Richard J.
- Plant Physiology, Vol. 125, Issue 1
Sequential Activation of Apical and Basolateral Contractility Drives Ascidian Endoderm Invagination
journal, September 2010
- Sherrard, Kristin; Robin, François; Lemaire, Patrick
- Current Biology, Vol. 20, Issue 17
Developmental Patterning by Mechanical Signals in Arabidopsis
journal, December 2008
- Hamant, O.; Heisler, M. G.; Jonsson, H.
- Science, Vol. 322, Issue 5908
Pulsed contractions of an actin–myosin network drive apical constriction
journal, November 2008
- Martin, Adam C.; Kaschube, Matthias; Wieschaus, Eric F.
- Nature, Vol. 457, Issue 7228
Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis
journal, August 2007
- Lecuit, Thomas; Lenne, Pierre-François
- Nature Reviews Molecular Cell Biology, Vol. 8, Issue 8