Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells

Sampathkumar, Arun; Krupinski, Pawel; Wightman, Raymond; Milani, Pascale; Berquand, Alexandre; Boudaoud, Arezki; Hamant, Olivier; Jönsson, Henrik; Meyerowitz, Elliot M.

doi:10.7554/eLife.01967

Title: Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells

Journal Article · Wed Apr 16 00:00:00 EDT 2014 · eLife

DOI:https://doi.org/10.7554/eLife.01967· OSTI ID:1197663

Sampathkumar, Arun; Krupinski, Pawel; Wightman, Raymond; Milani, Pascale; Berquand, Alexandre; Boudaoud, Arezki; Hamant, Olivier; Jönsson, Henrik; Meyerowitz, Elliot M.

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.

View Journal Article

Cite

Export

Save

Research Organization:: California Institute of Technology (CalTech), Pasadena, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: FG02-88ER13873

OSTI ID:: 1197663

Alternate ID(s):: OSTI ID: 1197668; OSTI ID: 1628807

Journal Information:: eLife, Journal Name: eLife Vol. 3; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 257 works

Citation information provided by
Web of Science

References (64)

A Mechanism for Reorientation of Cortical Microtubule Arrays Driven by Microtubule Severing Lindeboom, J. J.; Nakamura, M.; Hibbel, A. Science, Vol. 342, Issue 6163 https://doi.org/10.1126/science.1245533	journal	November 2013
Pulsed Forces Timed by a Ratchet-like Mechanism Drive Directed Tissue Movement during Dorsal Closure Solon, Jerome; Kaya-Çopur, Aynur; Colombelli, Julien Cell, Vol. 137, Issue 7 https://doi.org/10.1016/j.cell.2009.03.050	journal	June 2009
Experimental and theoretical study of mitotic spindle orientation Théry, Manuel; Jiménez-Dalmaroni, Andrea; Racine, Victor Nature, Vol. 447, Issue 7143 https://doi.org/10.1038/nature05786	journal	May 2007
Organogenesis-A Biophysical View Green, P. B. Annual Review of Plant Physiology, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.pp.31.060180.000411	journal	June 1980
The epidermal-growth-control theory of stem elongation: An old and a new perspective Kutschera, U.; Niklas, K. J. Journal of Plant Physiology, Vol. 164, Issue 11 https://doi.org/10.1016/j.jplph.2007.08.002	journal	November 2007
The growth speed of microtubules with XMAP215-coated beads coupled to their ends is increased by tensile force Trushko, Anastasiya; Schäffer, Erik; Howard, Jonathon Proceedings of the National Academy of Sciences, Vol. 110, Issue 36 https://doi.org/10.1073/pnas.1218053110	journal	August 2013
Mechanical feedback as a possible regulator of tissue growth Shraiman, B. I. Proceedings of the National Academy of Sciences, Vol. 102, Issue 9 https://doi.org/10.1073/pnas.0404782102	journal	February 2005
Effect of contact deformations on the adhesion of particles Derjaguin, B. V.; Muller, V. M.; Toporov, Yu. P. Journal of Colloid and Interface Science, Vol. 53, Issue 2 https://doi.org/10.1016/0021-9797(75)90018-1	journal	November 1975
Calibration of atomic‐force microscope tips Hutter, Jeffrey L.; Bechhoefer, John Review of Scientific Instruments, Vol. 64, Issue 7 https://doi.org/10.1063/1.1143970	journal	July 1993
Cell Polarity Signaling in Arabidopsis Yang, Zhenbiao Annual Review of Cell and Developmental Biology, Vol. 24, Issue 1 https://doi.org/10.1146/annurev.cellbio.23.090506.123233	journal	November 2008
Variability in the Control of Cell Division Underlies Sepal Epidermal Patterning in Arabidopsis thaliana Roeder, Adrienne H. K.; Chickarmane, Vijay; Cunha, Alexandre PLoS Biology, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pbio.1000367	journal	May 2010
Elastic Domains Regulate Growth and Organogenesis in the Plant Shoot Apical Meristem Kierzkowski, D.; Nakayama, N.; Routier-Kierzkowska, A. -L. Science, Vol. 335, Issue 6072 https://doi.org/10.1126/science.1213100	journal	March 2012
The Importance of Lattice Defects in Katanin-Mediated Microtubule Severing in Vitro Davis, Liza J.; Odde, David J.; Block, Steven M. Biophysical Journal, Vol. 82, Issue 6 https://doi.org/10.1016/S0006-3495(02)75632-4	journal	June 2002
Tension applied through the Dam1 complex promotes microtubule elongation providing a direct mechanism for length control in mitosis Franck, Andrew D.; Powers, Andrew F.; Gestaut, Daniel R. Nature Cell Biology, Vol. 9, Issue 7 https://doi.org/10.1038/ncb1609	journal	June 2007
Cell shaping and microtubules in developing mesophyll of wheat (Triticum aestivum L.) Jung, G.; Wernicke, W. Protoplasma, Vol. 153, Issue 3 https://doi.org/10.1007/BF01353998	journal	October 1990
Cell cycle regulates cell type in the Arabidopsis sepal Roeder, A. H. K.; Cunha, A.; Ohno, C. K. Development, Vol. 139, Issue 23 https://doi.org/10.1242/dev.082925	journal	October 2012
Cell Surface- and Rho GTPase-Based Auxin Signaling Controls Cellular Interdigitation in Arabidopsis Xu, Tongda; Wen, Mingzhang; Nagawa, Shingo Cell, Vol. 143, Issue 1 https://doi.org/10.1016/j.cell.2010.09.003	journal	October 2010
The Forces that Move Chromosomes in Mitosis Nicklas, R. B. Annual Review of Biophysics and Biophysical Chemistry, Vol. 17, Issue 1 https://doi.org/10.1146/annurev.bb.17.060188.002243	journal	June 1988
POM-POM2/CELLULOSE SYNTHASE INTERACTING1 Is Essential for the Functional Association of Cellulose Synthase and Microtubules in Arabidopsis Bringmann, Martin; Li, Eryang; Sampathkumar, Arun The Plant Cell, Vol. 24, Issue 1 https://doi.org/10.1105/tpc.111.093575	journal	January 2012
Biomechanics of plant growth Schopfer, P. American Journal of Botany, Vol. 93, Issue 10 https://doi.org/10.3732/ajb.93.10.1415	journal	October 2006
The rotation of cellulose synthase trajectories is microtubule dependent and influences the texture of epidermal cell walls in Arabidopsis hypocotyls Chan, J.; Crowell, E.; Eder, M. Journal of Cell Science, Vol. 123, Issue 20 https://doi.org/10.1242/jcs.074641	journal	September 2010
Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells: a push-pull mechanism Skibbens, R. V. The Journal of Cell Biology, Vol. 122, Issue 4 https://doi.org/10.1083/jcb.122.4.859	journal	August 1993
SPIRAL2 Determines Plant Microtubule Organization by Modulating Microtubule Severing Wightman, Raymond; Chomicki, Guillaume; Kumar, Manoj Current Biology, Vol. 23, Issue 19 https://doi.org/10.1016/j.cub.2013.07.061	journal	October 2013
Viscoelastic properties of cell walls of single living plant cells determined by dynamic nanoindentation Hayot, Céline M.; Forouzesh, Elham; Goel, Ashwani Journal of Experimental Botany, Vol. 63, Issue 7 https://doi.org/10.1093/jxb/err428	journal	January 2012
Differential Regulation of Cellulose Orientation at the Inner and Outer Face of Epidermal Cells in the Arabidopsis Hypocotyl Crowell, Elizabeth Faris; Timpano, Hélène; Desprez, Thierry The Plant Cell, Vol. 23, Issue 7 https://doi.org/10.1105/tpc.111.087338	journal	July 2011
Microtubule Severing at Crossover Sites by Katanin Generates Ordered Cortical Microtubule Arrays in Arabidopsis Zhang, Quan; Fishel, Erica; Bertroche, Tyler Current Biology, Vol. 23, Issue 21 https://doi.org/10.1016/j.cub.2013.09.018	journal	November 2013
Alignment between PIN1 Polarity and Microtubule Orientation in the Shoot Apical Meristem Reveals a Tight Coupling between Morphogenesis and Auxin Transport Heisler, Marcus G.; Hamant, Olivier; Krupinski, Pawel PLoS Biology, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pbio.1000516	journal	October 2010
The Relationship of Cells to Organisms in Plants: Problem and Implications of an Organismal Perspective Kaplan, Donald R. International Journal of Plant Sciences, Vol. 153, Issue 3, Part 2 https://doi.org/10.1086/297061	journal	September 1992
Arabidopsis Interdigitating Cell Growth Requires Two Antagonistic Pathways with Opposing Action on Cell Morphogenesis Fu, Ying; Gu, Ying; Zheng, Zhiliang Cell, Vol. 120, Issue 5 https://doi.org/10.1016/j.cell.2004.12.026	journal	March 2005
BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis Bichet, Adeline; Desnos, Thierry; Turner, Simon The Plant Journal, Vol. 25, Issue 2 https://doi.org/10.1046/j.1365-313x.2001.00946.x	journal	January 2001
The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile Sneddon, Ian N. International Journal of Engineering Science, Vol. 3, Issue 1 https://doi.org/10.1016/0020-7225(65)90019-4	journal	May 1965
Mechanical Stress Acts via Katanin to Amplify Differences in Growth Rate between Adjacent Cells in Arabidopsis Uyttewaal, Magalie; Burian, Agata; Alim, Karen Cell, Vol. 149, Issue 2 https://doi.org/10.1016/j.cell.2012.02.048	journal	April 2012
Onion epidermis as a new model to study the control of growth anisotropy in higher plants Suslov, D.; Verbelen, J. -P.; Vissenberg, K. Journal of Experimental Botany, Vol. 60, Issue 14 https://doi.org/10.1093/jxb/erp251	journal	August 2009
The mechanics behind cell polarity Asnacios, Atef; Hamant, Olivier Trends in Cell Biology, Vol. 22, Issue 11 https://doi.org/10.1016/j.tcb.2012.08.005	journal	November 2012
Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules Paredez, A. R. Science, Vol. 312, Issue 5779 https://doi.org/10.1126/science.1126551	journal	June 2006
Matrix Elasticity Directs Stem Cell Lineage Specification Engler, Adam J.; Sen, Shamik; Sweeney, H. Lee Cell, Vol. 126, Issue 4, p. 677-689 https://doi.org/10.1016/j.cell.2006.06.044	journal	August 2006
Regulation of Growth Anisotropy in Well-Watered and Water-Stressed Maize Roots. II. Role of Cortical Microtubules and Cellulose Microfibrils Baskin, Tobias I.; Meekes, Herman T. H. M.; Liang, Benjamin M. Plant Physiology, Vol. 119, Issue 2 https://doi.org/10.1104/pp.119.2.681	journal	February 1999
Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays: Microtubule dynamics Wightman, Raymond; Turner, Simon R. The Plant Journal, Vol. 52, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03271.x	journal	September 2007
Regulative feedback in pattern formation: towards a general relativistic theory of positional information Jaeger, J.; Irons, D.; Monk, N. Development, Vol. 135, Issue 19 https://doi.org/10.1242/dev.018697	journal	August 2008
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 Milani, Pascale; Gholamirad, Maryam; Traas, Jan The Plant Journal, Vol. 67, Issue 6 https://doi.org/10.1111/j.1365-313X.2011.04649.x	journal	July 2011
Rho GTPase Signaling Activates Microtubule Severing to Promote Microtubule Ordering in Arabidopsis Lin, Deshu; Cao, Lingyan; Zhou, Zhenzhen Current Biology, Vol. 23, Issue 4 https://doi.org/10.1016/j.cub.2013.01.022	journal	February 2013
Morphogen Gradient Formation Wartlick, O.; Kicheva, A.; Gonzalez-Gaitan, M. Cold Spring Harbor Perspectives in Biology, Vol. 1, Issue 3 https://doi.org/10.1101/cshperspect.a001255	journal	July 2009
An auxin-driven polarized transport model for phyllotaxis Jonsson, H.; Heisler, M. G.; Shapiro, B. E. Proceedings of the National Academy of Sciences, Vol. 103, Issue 5 https://doi.org/10.1073/pnas.0509839103	journal	January 2006
The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells Zhang, Chunhua; Halsey, Leah E.; Szymanski, Daniel B. BMC Plant Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2229-11-27	journal	January 2011
Tension-dependent Regulation of Microtubule Dynamics at Kinetochores Can Explain Metaphase Congression in Yeast Gardner, Melissa K.; Pearson, Chad G.; Sprague, Brian L. Molecular Biology of the Cell, Vol. 16, Issue 8 https://doi.org/10.1091/mbc.E05-04-0275	journal	August 2005
New Evidence for the Role of Mechanical Forces in the Shoot Apical Meristem Dumais, Jacques; Steele, Charles R. Journal of Plant Growth Regulation, Vol. 19, Issue 1 https://doi.org/10.1007/s003440000003	journal	March 2000
Finite element implementation of incompressible, transversely isotropic hyperelasticity Weiss, Jeffrey A.; Maker, Bradley N.; Govindjee, Sanjay Computer Methods in Applied Mechanics and Engineering, Vol. 135, Issue 1-2 https://doi.org/10.1016/0045-7825(96)01035-3	journal	August 1996
Mechanical properties of primary plant cell wall analogues Chanliaud, Elisabeth; Burrows, Kathleen; Jeronimidis, George Planta, Vol. 215, Issue 6 https://doi.org/10.1007/s00425-002-0783-8	journal	October 2002
Measuring the spring constant of atomic force microscope cantilevers: thermal fluctuations and other methods Lévy, R.; Maaloum, M. Nanotechnology, Vol. 13, Issue 1 https://doi.org/10.1088/0957-4484/13/1/307	journal	December 2001
Alignment of Cortical Microtubules by Anisotropic Wall Stresses Williamson, Re Functional Plant Biology, Vol. 17, Issue 6 https://doi.org/10.1071/PP9900601	journal	January 1990
Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis: Microtubules and cell-wall crystallinity Fujita, Miki; Himmelspach, Regina; Hocart, Charles H. The Plant Journal, Vol. 66, Issue 6 https://doi.org/10.1111/j.1365-313X.2011.04552.x	journal	April 2011
Positional information and the spatial pattern of cellular differentiation Wolpert, L. Journal of Theoretical Biology, Vol. 25, Issue 1 https://doi.org/10.1016/S0022-5193(69)80016-0	journal	October 1969
Mechanical Signals Trigger Myosin II Redistribution and Mesoderm Invagination in Drosophila Embryos Pouille, P. -A.; Ahmadi, P.; Brunet, A. -C. Science Signaling, Vol. 2, Issue 66 https://doi.org/10.1126/scisignal.2000098	journal	April 2009
Mechanical stress in Arabidopsis leaves orients microtubules in a 'continuous’ supracellular pattern Jacques, Eveline; Verbelen, Jean-Pierre; Vissenberg, Kris BMC Plant Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2229-13-163	journal	January 2013
FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images Boudaoud, Arezki; Burian, Agata; Borowska-Wykręt, Dorota Nature Protocols, Vol. 9, Issue 2 https://doi.org/10.1038/nprot.2014.024	journal	January 2014
Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors Stylianopoulos, T.; Martin, J. D.; Chauhan, V. P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 38 https://doi.org/10.1073/pnas.1213353109	journal	August 2012
Eukaryotic Cells and their Cell Bodies: Cell Theory Revised BALUsKA, F. Annals of Botany, Vol. 94, Issue 1 https://doi.org/10.1093/aob/mch109	journal	May 2004
Drosophila Katanin-60 Depolymerizes and Severs at Microtubule Defects Díaz-Valencia, Juan Daniel; Morelli, Margaret M.; Bailey, Megan Biophysical Journal, Vol. 100, Issue 10 https://doi.org/10.1016/j.bpj.2011.03.062	journal	May 2011
Quantification of the Young's modulus of the primary plant cell wall using Bending-Lab-On-Chip (BLOC) Nezhad, Amir Sanati; Naghavi, Mahsa; Packirisamy, Muthukumaran Lab on a Chip, Vol. 13, Issue 13 https://doi.org/10.1039/c3lc00012e	journal	January 2013
The Role of Microtubules in Guard Cell Function Marcus, Adam I.; Moore, Richard C.; Cyr, Richard J. Plant Physiology, Vol. 125, Issue 1 https://doi.org/10.1104/pp.125.1.387	journal	January 2001
Sequential Activation of Apical and Basolateral Contractility Drives Ascidian Endoderm Invagination Sherrard, Kristin; Robin, François; Lemaire, Patrick Current Biology, Vol. 20, Issue 17 https://doi.org/10.1016/j.cub.2010.06.075	journal	September 2010
Developmental Patterning by Mechanical Signals in Arabidopsis Hamant, O.; Heisler, M. G.; Jonsson, H. Science, Vol. 322, Issue 5908 https://doi.org/10.1126/science.1165594	journal	December 2008
Pulsed contractions of an actin–myosin network drive apical constriction Martin, Adam C.; Kaschube, Matthias; Wieschaus, Eric F. Nature, Vol. 457, Issue 7228 https://doi.org/10.1038/nature07522	journal	November 2008
Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis Lecuit, Thomas; Lenne, Pierre-François Nature Reviews Molecular Cell Biology, Vol. 8, Issue 8 https://doi.org/10.1038/nrm2222	journal	August 2007

Similar Records

Reassessing the roles of PIN proteins and anticlinal microtubules during pavement cell morphogenesis

Journal Article · Thu Nov 30 00:00:00 EST 2017 · Plant Physiology (Bethesda) · OSTI ID:1197663

Belteton, Samuel; Sawchuk, Megan G.; Donohoe, Bryon S.; +2 more

Arabidopsis pavement cell morphogenesis requires FERONIA binding to pectin for activation of ROP GTPase signaling

Journal Article · Tue Feb 01 00:00:00 EST 2022 · Current Biology · OSTI ID:1197663

Lin, Wenwei; Tang, Wenxin; Pan, Xue; +4 more

Analysis of cell division patterns in the Arabidopsis shoot apical meristem

Journal Article · Mon Mar 30 00:00:00 EDT 2015 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1197663

Shapiro, Bruce E.; Tobin, Cory; Mjolsness, Eric; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Life Sciences & Biomedicine - Other Topics

Title: Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells

Citation Formats

References (64)

Similar Records

Related Subjects