Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep
Abstract
De-esterification of homogalacturonan (HG) is thought to stiffen pectin gels and primary cell walls by increasing calcium cross-linking between HG chains. Contrary to this idea, recent studies found that HG de-esterification correlated with reduced stiffness of living tissues, measured by surface indentation. The physical basis of such apparent wall softening is unclear, but possibly involves complex biological responses to HG modification. To assess the direct physical consequences of HG de-esterification on wall mechanics without such complications, we treated isolated onion (Allium cepa) epidermal walls with pectin methylesterase (PME) and assessed wall biomechanics with indentation and tensile tests. In nanoindentation assays, PME action softened the wall (reduced the indentation modulus). In tensile force/extension assays, PME increased plasticity, but not elasticity. These softening effects are attributed, at least in part, to increased electrostatic repulsion and swelling of the wall after PME treatment. Despite softening and swelling upon HG de-esterification, PME treatment alone failed to induce cell wall creep. Instead, acid-induced creep, mediated by endogenous α-expansin, was reduced. We conclude that HG de-esterification physically softens the onion wall, yet reduces expansin-mediated wall extensibility.
- Authors:
-
- Pennsylvania State Univ., University Park, PA (United States)
- Publication Date:
- Research Org.:
- Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF); Pennsylvania State Univ., University Park, PA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1767734
- Grant/Contract Number:
- SC0001090
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Experimental Botany
- Additional Journal Information:
- Journal Volume: 71; Journal Issue: 9; Journal ID: ISSN 0022-0957
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; biofuels (including algae and biomass); bio-inspired; membrane; carbon sequestration; materials and chemistry by design; synthesis (self-assembly); atomic force microscopy; biomechanics; expansin; homogalacturonan; nanoindentation; onion (Allium cepa) epidermis; pectin methylesterase; plant cell wall mechanics; tensile testing; wall hydration
Citation Formats
Wang, Xuan, Wilson, Liza, and Cosgrove, Daniel J. Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep. United States: N. p., 2020.
Web. doi:10.1093/jxb/eraa059.
Wang, Xuan, Wilson, Liza, & Cosgrove, Daniel J. Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep. United States. https://doi.org/10.1093/jxb/eraa059
Wang, Xuan, Wilson, Liza, and Cosgrove, Daniel J. Sat .
"Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep". United States. https://doi.org/10.1093/jxb/eraa059. https://www.osti.gov/servlets/purl/1767734.
@article{osti_1767734,
title = {Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep},
author = {Wang, Xuan and Wilson, Liza and Cosgrove, Daniel J.},
abstractNote = {De-esterification of homogalacturonan (HG) is thought to stiffen pectin gels and primary cell walls by increasing calcium cross-linking between HG chains. Contrary to this idea, recent studies found that HG de-esterification correlated with reduced stiffness of living tissues, measured by surface indentation. The physical basis of such apparent wall softening is unclear, but possibly involves complex biological responses to HG modification. To assess the direct physical consequences of HG de-esterification on wall mechanics without such complications, we treated isolated onion (Allium cepa) epidermal walls with pectin methylesterase (PME) and assessed wall biomechanics with indentation and tensile tests. In nanoindentation assays, PME action softened the wall (reduced the indentation modulus). In tensile force/extension assays, PME increased plasticity, but not elasticity. These softening effects are attributed, at least in part, to increased electrostatic repulsion and swelling of the wall after PME treatment. Despite softening and swelling upon HG de-esterification, PME treatment alone failed to induce cell wall creep. Instead, acid-induced creep, mediated by endogenous α-expansin, was reduced. We conclude that HG de-esterification physically softens the onion wall, yet reduces expansin-mediated wall extensibility.},
doi = {10.1093/jxb/eraa059},
journal = {Journal of Experimental Botany},
number = 9,
volume = 71,
place = {United States},
year = {Sat Feb 01 00:00:00 EST 2020},
month = {Sat Feb 01 00:00:00 EST 2020}
}
Works referenced in this record:
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
Cell wall mechanics and growth control in plants: the role of pectins revisited
journal, January 2012
- Peaucelle, Alexis; Braybrook, Siobhan; Höfte, Herman
- Frontiers in Plant Science, Vol. 3
Calibration of atomic‐force microscope tips
journal, July 1993
- Hutter, Jeffrey L.; Bechhoefer, John
- Review of Scientific Instruments, Vol. 64, Issue 7
Nanoscale structure, mechanics and growth of epidermal cell walls
journal, December 2018
- Cosgrove, Daniel J.
- Current Opinion in Plant Biology, Vol. 46
Biomechanical Characterization of Onion Epidermal Cell Walls
journal, January 2017
- Durachko, Daniel; Park, Yong Bum; Zhang, Tian
- BIO-PROTOCOL, Vol. 7, Issue 24
Demethylesterification of the Primary Wall by PECTIN METHYLESTERASE35 Provides Mechanical Support to the Arabidopsis Stem
journal, June 2012
- Hongo, Shoko; Sato, Kaori; Yokoyama, Ryusuke
- The Plant Cell, Vol. 24, Issue 6
Determining the polysaccharide composition of plant cell walls
journal, August 2012
- Pettolino, Filomena A.; Walsh, Cherie; Fincher, Geoffrey B.
- Nature Protocols, Vol. 7, Issue 9
Dissipation and strain-stiffening behavior of pectin–Ca gels under LAOS
journal, January 2019
- John, Jacob; Ray, Debes; Aswal, Vinod K.
- Soft Matter, Vol. 15, Issue 34
Calcium gelation of pectic polysaccharides isolated from unripe tomato fruit
journal, October 1996
- MacDougall, Alistair J.; Needs, Paul W.; Rigby, Neil M.
- Carbohydrate Research, Vol. 293, Issue 2
How do cell walls regulate plant growth?
journal, August 2005
- Thompson, David Stuart
- Journal of Experimental Botany, Vol. 56, Issue 419
Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls
journal, September 2013
- Wang, T.; Park, Y. B.; Caporini, M. A.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 41
Swelling Behavior of the Tomato Cell Wall Network
journal, June 2001
- MacDougall, Alistair J.; Rigby, Neil M.; Ryden, Peter
- Biomacromolecules, Vol. 2, Issue 2
Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy
journal, January 2016
- Zhang, Tian; Zheng, Yunzhen; Cosgrove, Daniel J.
- The Plant Journal, Vol. 85, Issue 2
Determination of methanol using alcohol oxidase and its application to methyl ester content of pectins
journal, July 1986
- Klavons, Jerome A.; Bennett, Raymond D.
- Journal of Agricultural and Food Chemistry, Vol. 34, Issue 4
Electrostatic effects and the dynamics of enzyme reactions at the surface of plant cells. 2. The role of pectin methyl esterase in the modulation of electrostatic effects in soybean cell walls
journal, February 1986
- Moustacas, Anne-Marie; Nari, Johanes; Diamantidis, Gregoire
- European Journal of Biochemistry, Vol. 155, Issue 1
Pectin methylesterase, metal ions and plant cell-wall extension. The role of metal ions in plant cell-wall extension
journal, October 1991
- Moustacas, A. M.; Nari, J.; Borel, M.
- Biochemical Journal, Vol. 279, Issue 2
Dynamics of multi-enzyme reactions, cell growth and perception of ionic signals from the external milieu
journal, October 1987
- Ricard, Jacques
- Journal of Theoretical Biology, Vol. 128, Issue 3
The Control of Growth Symmetry Breaking in the Arabidopsis Hypocotyl
journal, June 2015
- Peaucelle, Alexis; Wightman, Raymond; Höfte, Herman
- Current Biology, Vol. 25, Issue 13
Pectin Methyl Esterase Inhibits Intrusive and Symplastic Cell Growth in Developing Wood Cells of Populus
journal, December 2007
- Siedlecka, Anna; Wiklund, Susanne; Péronne, Marie-Amélie
- Plant Physiology, Vol. 146, Issue 2
Plant Cell Wall Homeostasis Is Mediated by Brassinosteroid Feedback Signaling
journal, September 2012
- Wolf, Sebastian; Mravec, Jozef; Greiner, Steffen
- Current Biology, Vol. 22, Issue 18
Chain association of pectic molecules during calcium-induced gelation
journal, March 1986
- Thibault, J. F.; Rinaudo, M.
- Biopolymers, Vol. 25, Issue 3
Disentangling loosening from softening: insights into primary cell wall structure
journal, September 2019
- Zhang, Tian; Tang, Haosu; Vavylonis, Dimitrios
- The Plant Journal, Vol. 100, Issue 6
A tension-adhesion feedback loop in plant epidermis
journal, April 2018
- Verger, Stéphane; Long, Yuchen; Boudaoud, Arezki
- eLife, Vol. 7
A Revised Architecture of Primary Cell Walls Based on Biomechanical Changes Induced by Substrate-Specific Endoglucanases
journal, February 2012
- Park, Yong Bum; Cosgrove, Daniel J.
- Plant Physiology, Vol. 158, Issue 4
Shrinking the hammer: micromechanical approaches to morphogenesis
journal, July 2013
- Milani, Pascale; Braybrook, Siobhan A.; Boudaoud, Arezki
- Journal of Experimental Botany, Vol. 64, Issue 15
Catalysts of plant cell wall loosening
journal, January 2016
- Cosgrove, Daniel J.
- F1000Research, Vol. 5
Autolysis and extension of isolated walls from growing cucumber hypocotyls
journal, November 1994
- Cosgrove, Daniel J.; Durachko, Daniel M.
- Journal of Experimental Botany, Vol. 45, Issue Special_Issue
Developing a ‘thick skin’: a paradoxical role for mechanical tension in maintaining epidermal integrity?
journal, September 2016
- Galletti, Roberta; Verger, Stéphane; Hamant, Olivier
- Development, Vol. 143, Issue 18
Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR
journal, October 2018
- Phyo, Pyae; Gu, Ying; Hong, Mei
- Cellulose, Vol. 26, Issue 1
Synergism between cucumber α-expansin, fungal endoglucanase and pectin lyase
journal, September 2010
- Wei, Wei; Yang, Chun; Luo, Jun
- Journal of Plant Physiology, Vol. 167, Issue 14
Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties
journal, October 2009
- Zerzour, Rabah; Kroeger, Jens; Geitmann, Anja
- Developmental Biology, Vol. 334, Issue 2
Atomic force microscopy based nanoindentation study of onion abaxial epidermis walls in aqueous environment
journal, January 2015
- Xi, Xiaoning; Kim, Seong H.; Tittmann, Bernhard
- Journal of Applied Physics, Vol. 117, Issue 2
Nanostructure and poroviscoelasticity in cell wall materials from onion, carrot and apple: Roles of pectin
journal, January 2020
- Lopez-Sanchez, P.; Martinez-Sanz, M.; Bonilla, M. R.
- Food Hydrocolloids, Vol. 98
Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis Primary Cell Walls: Evidence from Solid-State Nuclear Magnetic Resonance
journal, June 2015
- Wang, Tuo; Park, Yong Bum; Cosgrove, Daniel J.
- Plant Physiology, Vol. 168, Issue 3
Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis
journal, July 2013
- Zhang, Tian; Mahgsoudy-Louyeh, Sahar; Tittmann, Bernhard
- Cellulose, Vol. 21, 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
Modulation of the Degree and Pattern of Methyl-esterification of Pectic Homogalacturonan in Plant Cell Walls: IMPLICATIONS FOR PECTIN METHYL ESTERASE ACTION, MATRIX PROPERTIES, AND CELL ADHESION
journal, March 2001
- Willats, William G. T.; Orfila, Caroline; Limberg, Gerrit
- Journal of Biological Chemistry, Vol. 276, Issue 22
The Cell Wall of the Arabidopsis Pollen Tube—Spatial Distribution, Recycling, and Network Formation of Polysaccharides
journal, October 2012
- Chebli, Youssef; Kaneda, Minako; Zerzour, Rabah
- Plant Physiology, Vol. 160, Issue 4
Cell wall water content has a direct effect on extensibility in growing hypocotyls of sunflower (Helianthus annuus L.)
journal, September 2007
- Evered, Carol; Majevadia, Bhavita; Thompson, David Stuart
- Journal of Experimental Botany, Vol. 58, Issue 12
The role of wall calcium in the extension of cell walls of soybean hypocotyls
journal, November 1990
- Virk, Sarbjit S.; Cleland, Robert E.
- Planta, Vol. 182, Issue 4
Pectin-Induced Changes in Cell Wall Mechanics Underlie Organ Initiation in Arabidopsis
journal, October 2011
- Peaucelle, Alexis; Braybrook, Siobhan A.; Le Guillou, Laurent
- Current Biology, Vol. 21, Issue 20
Restoration of Mature Etiolated Cucumber Hypocotyl Cell Wall Susceptibility to Expansin by Pretreatment with Fungal Pectinases and EGTA in Vitro
journal, June 2008
- Zhao, Qingxin; Yuan, Sheng; Wang, Xin
- Plant Physiology, Vol. 147, Issue 4
Control of thickness of collenchyma cell walls by pectins
journal, May 1992
- Jarvis, M. C.
- Planta, Vol. 187, Issue 2
Conformations and interactions of pectins
journal, March 1982
- Morris, E. R.; Powell, D. A.; Gidley, M. J.
- Journal of Molecular Biology, Vol. 155, Issue 4
Homogalacturonan Methyl-Esterification and Plant Development
journal, September 2009
- Wolf, Sebastian; Mouille, Grégory; Pelloux, Jérome
- Molecular Plant, Vol. 2, Issue 5
The Role of the Epidermis in the Control of Elongation Growth in Stems and Coleoptiles
journal, August 1992
- Kutschera, U.
- Botanica Acta, Vol. 105, Issue 4
Diffuse Growth of Plant Cell Walls
journal, November 2017
- Cosgrove, Daniel J.
- Plant Physiology, Vol. 176, Issue 1
Evolving Views of Pectin Biosynthesis
journal, April 2013
- Atmodjo, Melani A.; Hao, Zhangying; Mohnen, Debra
- Annual Review of Plant Biology, Vol. 64, Issue 1
Nanoscale movements of cellulose microfibrils in primary cell walls
journal, April 2017
- Zhang, Tian; Vavylonis, Dimitrios; Durachko, Daniel M.
- Nature Plants, Vol. 3, Issue 5
Arabidopsis Phyllotaxis Is Controlled by the Methyl-Esterification Status of Cell-Wall Pectins
journal, December 2008
- Peaucelle, Alexis; Louvet, Romain; Johansen, Jorunn N.
- Current Biology, Vol. 18, Issue 24
Mechano-Chemical Aspects of Organ Formation in Arabidopsis thaliana: The Relationship between Auxin and Pectin
journal, March 2013
- Braybrook, Siobhan A.; Peaucelle, Alexis
- PLoS ONE, Vol. 8, Issue 3
Tuning of pectin methylesterification: consequences for cell wall biomechanics and development
journal, July 2015
- Levesque-Tremblay, Gabriel; Pelloux, Jerome; Braybrook, Siobhan A.
- Planta, Vol. 242, Issue 4
Hydration of pectic polysaccharides
journal, January 2000
- Ryden, P.; MacDougall, A. J.; Tibbits, C. W.
- Biopolymers, Vol. 54, Issue 6
Material properties of concentrated pectin networks
journal, May 2004
- Zsivanovits, Gabor; MacDougall, Alistair J.; Smith, Andrew C.
- Carbohydrate Research, Vol. 339, Issue 7
Force measurements with the atomic force microscope: Technique, interpretation and applications
journal, October 2005
- Butt, Hans-Jürgen; Cappella, Brunero; Kappl, Michael
- Surface Science Reports, Vol. 59, Issue 1-6
An extended set of monoclonal antibodies to pectic homogalacturonan
journal, September 2009
- Verhertbruggen, Yves; Marcus, Susan E.; Haeger, Ash
- Carbohydrate Research, Vol. 344, Issue 14
Pectin Metabolism and Assembly in the Cell Wall of the Charophyte Green Alga Penium margaritaceum
journal, March 2014
- Domozych, David S.; Sørensen, Iben; Popper, Zoë A.
- Plant Physiology, Vol. 165, Issue 1
Mathematical principles and models of plant growth mechanics: from cell wall dynamics to tissue morphogenesis
journal, May 2019
- Smithers, Euan T.; Luo, Jingxi; Dyson, Rosemary J.
- Journal of Experimental Botany, Vol. 70, Issue 14
Water Potential Modulates Extensibility of Rye Coleoptile Cell Walls
journal, August 1995
- Edelmann, H. G.
- Botanica Acta, Vol. 108, Issue 4
Studies on the Role of Wall Extensibility in the Control of Cell Expansion
journal, March 1980
- Coartney, James S.; Morre, D. James
- Botanical Gazette, Vol. 141, Issue 1
In vivo extraction of Arabidopsis cell turgor pressure using nanoindentation in conjunction with finite element modeling
journal, December 2012
- Forouzesh, Elham; Goel, Ashwani; Mackenzie, Sally A.
- The Plant Journal, Vol. 73, Issue 3
Anisotropic growth is achieved through the additive mechanical effect of material anisotropy and elastic asymmetry
journal, September 2018
- Bou Daher, Firas; Chen, Yuanjie; Bozorg, Behruz
- eLife, Vol. 7
Measuring the mechanical properties of plant cells by combining micro-indentation with osmotic treatments
journal, April 2015
- Weber, Alain; Braybrook, Siobhan; Huflejt, Michal
- Journal of Experimental Botany, Vol. 66, Issue 11
Connecting Homogalacturonan-Type Pectin Remodeling to Acid Growth
journal, January 2017
- Hocq, Ludivine; Pelloux, Jérôme; Lefebvre, Valérie
- Trends in Plant Science, Vol. 22, Issue 1
Gradients in Wall Mechanics and Polysaccharides along Growing Inflorescence Stems
journal, October 2017
- Phyo, Pyae; Wang, Tuo; Kiemle, Sarah N.
- Plant Physiology, Vol. 175, Issue 4
Structure and Properties of Acidic Polysaccharides from Mung Bean Hypocotyls
journal, March 1989
- Goldberg, Renée; Morvan, Claudine; du Penhoat, Catherine Hervé
- Plant and Cell Physiology, Vol. 30, Issue 2
Conformations and interactions of pectins
journal, March 1982
- Powell, D. A.; Morris, E. R.; Gidley, M. J.
- Journal of Molecular Biology, Vol. 155, Issue 4
Two Endogenous Proteins That Induce Cell Wall Extension in Plants
journal, November 1992
- McQueen-Mason, Simon; Durachko, Daniel M.; Cosgrove, Daniel J.
- The Plant Cell, Vol. 4, Issue 11
Measuring the mechanical properties of plant cells by combining micro-indentation with osmotic treatments
text, January 2015
- Weber, Alain; Braybrook, Siobhan; Huflejt, Michal
- Oxford University Press
The Control of Growth Symmetry Breaking in the Arabidopsis Hypocotyl
journal, June 2015
- Peaucelle, Alexis; Wightman, Raymond; Höfte, Herman
- Current Biology, Vol. 25, Issue 13
Two endogenous proteins that induce cell wall extension in plants.
journal, November 1992
- McQueen-Mason, S.; Durachko, D. M.; Cosgrove, D. J.
- The Plant Cell, Vol. 4, Issue 11
Anisotropic growth is achieved through the additive mechanical effect of material anisotropy and elastic asymmetry.
text, January 2018
- Bou Daher, Firas; Chen, Yuanjie; Bozorg, Behruz
- Apollo - University of Cambridge Repository
Studies on the Role of Wall Extensibility in the Control of Cell Expansion
journal, March 1980
- Coartney, James S.; Morre, D. James
- Botanical Gazette, Vol. 141, Issue 1
Mechano-Chemical Aspects of Organ Formation in Arabidopsis thaliana: The Relationship between Auxin and Pectin
journal, March 2013
- Braybrook, Siobhan A.; Peaucelle, Alexis
- PLoS ONE, Vol. 8, Issue 3
Anisotropic growth is achieved through the additive mechanical effect of material anisotropy and elastic asymmetry.
text, January 2018
- Bou Daher, Firas; Chen, Yuanjie; Bozorg, Behruz
- Apollo - University of Cambridge Repository