Disentangling loosening from softening: insights into primary cell wall structure

Zhang, Tian; Tang, Haosu; Vavylonis, Dimitrios; Cosgrove, Daniel J.

doi:10.1111/tpj.14519

Title: Disentangling loosening from softening: insights into primary cell wall structure

Abstract

How cell wall elasticity, plasticity, and time-dependent extension (creep) relate to one another, to plant cell wall structure and to cell growth remain unsettled topics. To examine these issues without the complexities of living tissues, in this work we treated cell-free strips of onion epidermal walls with various enzymes and other agents to assess which polysaccharides bear mechanical forces in-plane and out-of-plane of the cell wall. This information is critical for integrating concepts of wall structure, wall material properties, tissue mechanics, and mechanisms of cell growth. With atomic force microscopy we also monitored real-time changes in the wall surface during treatments. Driselase, a potent cocktail of wall-degrading enzymes, removed cellulose microfibrils in superficial lamellae sequentially, layer-by-layer, and softened the wall (reduced its mechanical stiffness), yet did not induce wall loosening (creep). In contrast Cel12A, a bifunctional xyloglucanase/cellulase, induced creep with only subtle changes in wall appearance. Both Driselase and Cel12A increased the tensile compliance, but differently for elastic and plastic components. Homogalacturonan solubilization by pectate lyase and calcium chelation greatly increased the indentation compliance without changing tensile compliances. Acidic buffer induced rapid cell wall creep via endogenous α-expansins, with negligible effects on wall compliances. We conclude that these various wallmore »« less

Authors:

Zhang, Tian ^[1]; Tang, Haosu ^[2]; Vavylonis, Dimitrios ^[2];

^[1]

Pennsylvania State Univ., University Park, PA (United States). Dept. of Biology and Center for Lignocellulose Structure and Formation
Lehigh Univ., Bethlehem, PA (United States). Dept. of Physics

Publication Date:: Fri Aug 30 00:00:00 EDT 2019

Research Org.:: Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF); Pennsylvania State Univ., University Park, PA (United States); Lehigh Univ., Bethlehem, PA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1595717

Alternate Identifier(s):: OSTI ID: 1567708

Grant/Contract Number:: SC0001090

Resource Type:: Accepted Manuscript

Journal Name:: The Plant Journal

Additional Journal Information:: Journal Volume: 100; Journal Issue: 6; Journal ID: ISSN 0960-7412

Publisher:: Society for Experimental Biology

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; biomechanics of primary cell walls; atomic force microscopy (AFM); Cel12A endoglucanase; driselase; cellulose; expansin; nano-indentation; onion (Allium cepa) epidermal cell wall; homogalacturonan; pectate lyase

Citation Formats


                    Zhang, Tian, Tang, Haosu, Vavylonis, Dimitrios, and Cosgrove, Daniel J. Disentangling loosening from softening: insights into primary cell wall structure.  United States: N. p., 2019. 
Web.  doi:10.1111/tpj.14519.

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                    Zhang, Tian, Tang, Haosu, Vavylonis, Dimitrios, & Cosgrove, Daniel J. Disentangling loosening from softening: insights into primary cell wall structure.  United States.  https://doi.org/10.1111/tpj.14519

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                    Zhang, Tian, Tang, Haosu, Vavylonis, Dimitrios, and Cosgrove, Daniel J. Fri .  
"Disentangling loosening from softening: insights into primary cell wall structure".  United States.  https://doi.org/10.1111/tpj.14519.  https://www.osti.gov/servlets/purl/1595717.

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@article{osti_1595717,

  title        = {Disentangling loosening from softening: insights into primary cell wall structure},

  author       = {Zhang, Tian and Tang, Haosu and Vavylonis, Dimitrios and Cosgrove, Daniel J.},

  abstractNote = {How cell wall elasticity, plasticity, and time-dependent extension (creep) relate to one another, to plant cell wall structure and to cell growth remain unsettled topics. To examine these issues without the complexities of living tissues, in this work we treated cell-free strips of onion epidermal walls with various enzymes and other agents to assess which polysaccharides bear mechanical forces in-plane and out-of-plane of the cell wall. This information is critical for integrating concepts of wall structure, wall material properties, tissue mechanics, and mechanisms of cell growth. With atomic force microscopy we also monitored real-time changes in the wall surface during treatments. Driselase, a potent cocktail of wall-degrading enzymes, removed cellulose microfibrils in superficial lamellae sequentially, layer-by-layer, and softened the wall (reduced its mechanical stiffness), yet did not induce wall loosening (creep). In contrast Cel12A, a bifunctional xyloglucanase/cellulase, induced creep with only subtle changes in wall appearance. Both Driselase and Cel12A increased the tensile compliance, but differently for elastic and plastic components. Homogalacturonan solubilization by pectate lyase and calcium chelation greatly increased the indentation compliance without changing tensile compliances. Acidic buffer induced rapid cell wall creep via endogenous α-expansins, with negligible effects on wall compliances. We conclude that these various wall properties are not tightly coupled and thus reflect distinctive aspects of wall structure. Cross-lamellate networks of cellulose microfibrils influenced creep and tensile stiffness whereas homogalacturonan influenced indentation mechanics. This information is crucial for constructing realistic molecular models that define how wall mechanics and growth depend on primary cell wall structure.},

  doi          = {10.1111/tpj.14519},

  journal      = {The Plant Journal},

  number       = 6,

  volume       = 100,

  place        = {United States},

  year         = {Fri Aug 30 00:00:00 EDT 2019},

  month        = {Fri Aug 30 00:00:00 EDT 2019}

}

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Anisotropic growth is achieved through the additive mechanical effect of material anisotropy and elastic asymmetry.
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Apollo - University of Cambridge Repository
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An automated confocal micro-extensometer enables in vivo quantification of mechanical properties with cellular resolution.
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Works referencing / citing this record:

Combining tensile testing and microscopy to address a diverse range of questions
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Journal of Experimental Botany, Vol. 71, Issue 9
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Title: Disentangling loosening from softening: insights into primary cell wall structure

Abstract

Citation Formats

Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls journal, September 2015

Rapid and reversible root growth inhibition by TIR1 auxin signalling journal, June 2018

Biomechanical Characterization of Onion Epidermal Cell Walls journal, January 2017

Salinity Stiffens the Epidermal Cell Walls of Salt-Stressed Maize Leaves: Is the Epidermis Growth-Restricting? journal, March 2015

Quantifying Hydrostatic Pressure in Plant Cells by Using Indentation with an Atomic Force Microscope journal, May 2015

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Physical extensibility of maize coleoptile cell walls: apparent plastic extensibility is due to elastic hysteresis journal, July 1992

Finite Element Modeling of Shape Changes in Plant Cells journal, December 2017

Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy journal, January 2016

Growth of the plant cell wall journal, November 2005

The Control of Growth Symmetry Breaking in the Arabidopsis Hypocotyl journal, June 2015

Molecular dynamics simulation study of xyloglucan adsorption on cellulose surfaces: effects of surface hydrophobicity and side-chain variation journal, September 2013

Pectin Chemistry and Cellulose Crystallinity Govern Pavement Cell Morphogenesis in a Multi-Step Mechanism journal, July 2019

The Instron technique as a measure of immediate-past wall extensibility journal, May 1984

A Revised Architecture of Primary Cell Walls Based on Biomechanical Changes Induced by Substrate-Specific Endoglucanases journal, February 2012

Xyloglucan Deficiency Disrupts Microtubule Stability and Cellulose Biosynthesis in Arabidopsis, Altering Cell Growth and Morphogenesis journal, November 2015

Autolysis and extension of isolated walls from growing cucumber hypocotyls journal, November 1994

Cellular growth in plants requires regulation of cell wall biochemistry journal, February 2017

Shifting foundations: the mechanical cell wall and development journal, February 2016

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

Polysaccharide Conformation and Cell Wall Function journal, June 1979

Atomic force microscopy based nanoindentation study of onion abaxial epidermis walls in aqueous environment journal, January 2015

Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells journal, April 2014

Size, shape, and arrangement of native cellulose fibrils in maize cell walls journal, December 2013

Segmentation and tracking of cytoskeletal filaments using open active contours journal, October 2010

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

Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls journal, January 1989

The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile journal, May 1965

The Structure and Plastic Properties of the Cell Wall of Nitella in Relation to Extension Growth journal, January 1966

Pectin-Induced Changes in Cell Wall Mechanics Underlie Organ Initiation in Arabidopsis journal, October 2011

Restoration of Mature Etiolated Cucumber Hypocotyl Cell Wall Susceptibility to Expansin by Pretreatment with Fungal Pectinases and EGTA in Vitro journal, June 2008

Control of thickness of collenchyma cell walls by pectins journal, May 1992

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

How Does Plant Cell Wall Nanoscale Architecture Correlate with Enzymatic Digestibility? journal, November 2012

A Fungal Endoglucanase with Plant Cell Wall Extension Activity journal, September 2001

The mechanical properties of plant cell walls soft material at the subcellular scale: the implications of water and of the intercellular boundaries journal, July 2015

Continually emerging mechanistic complexity of the multi-enzyme cellulosome complex journal, June 2017

Long-term acid-induced wall extension in an in-vitro system journal, March 1987

Physicochemical Characteristics of Onion ( Allium cepa L.) Tissues journal, November 2000

Nanoscale movements of cellulose microfibrils in primary cell walls journal, April 2017

Measuring the mechanics of morphogenesis journal, February 2013

Colorimetric Method for Determination of Sugars and Related Substances journal, March 1956

Mode of Action of Exo- and Endo-Type Cellulases from Irpex lacteus in the Hydrolysis of Cellulose with Different Crystallinities journal, August 1993

Restricted access of proteins to mannan polysaccharides in intact plant cell walls: Masking of mannan polysaccharides journal, August 2010

Electron Tomography of Cryo-Immobilized Plant Tissue: A Novel Approach to Studying 3D Macromolecular Architecture of Mature Plant Cell Walls In Situ journal, September 2014

A synthetic biology approach for evaluating the functional contribution of designer cellulosome components to deconstruction of cellulosic substrates journal, January 2013

Nanoscale structure, mechanics and growth of epidermal cell walls journal, December 2018

The Growing Outer Epidermal Wall: Design and Physiological Role of a Composite Structure journal, February 2008

Dual-axis electron tomography: a new approach for investigating the spatial organization of wood cellulose microfibrils journal, July 2006

Cellular Force Microscopy for in Vivo Measurements of Plant Tissue Mechanics journal, February 2012

Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls journal, September 2013

Mechanochemical Polarization of Contiguous Cell Walls Shapes Plant Pavement Cells journal, November 2017

Changes in Cell Wall Biomechanical Properties in the Xyloglucan-Deficient xxt1/xxt2 Mutant of Arabidopsis journal, November 2011

Why plants make puzzle cells, and how their shape emerges journal, February 2018

Architecture-Based Multiscale Computational Modeling of Plant Cell Wall Mechanics to Examine the Hydrogen-Bonding Hypothesis of the Cell Wall Network Structure Model journal, August 2012

Extensibility of isolated cell walls: Measurement and changes during cell elongation journal, January 1967

Multiscale stress-strain characterization of onion outer epidermal tissue in wet and dry states journal, January 2015

Shrinking the hammer: micromechanical approaches to morphogenesis journal, July 2013

Plant expansins: diversity and interactions with plant cell walls journal, June 2015

Mechanical characterization of outer epidermal middle lamella of onion under tensile loading journal, May 2014

Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis journal, March 2015

Synergism between cucumber α-expansin, fungal endoglucanase and pectin lyase journal, September 2010

Differential Regulation of Cellulose Orientation at the Inner and Outer Face of Epidermal Cells in the Arabidopsis Hypocotyl journal, July 2011

Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides journal, December 2016

3D Electron Tomography of Pretreated Biomass Informs Atomic Modeling of Cellulose Microfibrils journal, August 2013

On the role of stress anisotropy in the growth of stems journal, August 2013

TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls journal, September 2016

An oat coleoptile wall protein that induces wall extension in vitro and that is antigenically related to a similar protein from cucumber hypocotyls journal, August 1993

Loosening of plant cell walls by expansins journal, September 2000

Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis Primary Cell Walls: Evidence from Solid-State Nuclear Magnetic Resonance journal, June 2015

Preparation of Onion Epidermal Cell Walls for Imaging by Atomic Force Microscopy (AFM) journal, January 2017

Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes journal, November 2015

WallGen, Software to Construct Layered Cellulose-Hemicellulose Networks and Predict Their Small Deformation Mechanics journal, December 2009

Disrupting Two Arabidopsis thaliana Xylosyltransferase Genes Results in Plants Deficient in Xyloglucan, a Major Primary Cell Wall Component journal, June 2008

Effects of mechanical stretching on average orientation of cellulose and pectin in onion epidermis cell wall: A polarized FT-IR study journal, May 2017

Assessment of In Vitro Binding of Isolated Pectic Domains to Cellulose by Adsorption Isotherms, Electron Microscopy, and X-ray Diffraction Methods journal, January 2007

On the micro-indentation of plant cells in a tissue context journal, February 2017

Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls
journal, September 2015

Rapid and reversible root growth inhibition by TIR1 auxin signalling
journal, June 2018

Biomechanical Characterization of Onion Epidermal Cell Walls
journal, January 2017

Salinity Stiffens the Epidermal Cell Walls of Salt-Stressed Maize Leaves: Is the Epidermis Growth-Restricting?
journal, March 2015

Quantifying Hydrostatic Pressure in Plant Cells by Using Indentation with an Atomic Force Microscope
journal, May 2015

Regulation of plant cell wall stiffness by mechanical stress: a mesoscale physical model
journal, September 2018

Physical extensibility of maize coleoptile cell walls: apparent plastic extensibility is due to elastic hysteresis
journal, July 1992

Finite Element Modeling of Shape Changes in Plant Cells
journal, December 2017

Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy
journal, January 2016

Growth of the plant cell wall
journal, November 2005

The Control of Growth Symmetry Breaking in the Arabidopsis Hypocotyl
journal, June 2015

Molecular dynamics simulation study of xyloglucan adsorption on cellulose surfaces: effects of surface hydrophobicity and side-chain variation
journal, September 2013

Pectin Chemistry and Cellulose Crystallinity Govern Pavement Cell Morphogenesis in a Multi-Step Mechanism
journal, July 2019

The Instron technique as a measure of immediate-past wall extensibility
journal, May 1984

A Revised Architecture of Primary Cell Walls Based on Biomechanical Changes Induced by Substrate-Specific Endoglucanases
journal, February 2012

Xyloglucan Deficiency Disrupts Microtubule Stability and Cellulose Biosynthesis in Arabidopsis, Altering Cell Growth and Morphogenesis
journal, November 2015

Autolysis and extension of isolated walls from growing cucumber hypocotyls
journal, November 1994

Cellular growth in plants requires regulation of cell wall biochemistry
journal, February 2017

Shifting foundations: the mechanical cell wall and development
journal, February 2016

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

Polysaccharide Conformation and Cell Wall Function
journal, June 1979

Atomic force microscopy based nanoindentation study of onion abaxial epidermis walls in aqueous environment
journal, January 2015

Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells
journal, April 2014

Size, shape, and arrangement of native cellulose fibrils in maize cell walls
journal, December 2013

Segmentation and tracking of cytoskeletal filaments using open active contours
journal, October 2010

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

Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls
journal, January 1989

The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile
journal, May 1965

The Structure and Plastic Properties of the Cell Wall of Nitella in Relation to Extension Growth
journal, January 1966

Pectin-Induced Changes in Cell Wall Mechanics Underlie Organ Initiation in Arabidopsis
journal, October 2011

Restoration of Mature Etiolated Cucumber Hypocotyl Cell Wall Susceptibility to Expansin by Pretreatment with Fungal Pectinases and EGTA in Vitro
journal, June 2008

Control of thickness of collenchyma cell walls by pectins
journal, May 1992

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

How Does Plant Cell Wall Nanoscale Architecture Correlate with Enzymatic Digestibility?
journal, November 2012

A Fungal Endoglucanase with Plant Cell Wall Extension Activity
journal, September 2001

The mechanical properties of plant cell walls soft material at the subcellular scale: the implications of water and of the intercellular boundaries
journal, July 2015

Continually emerging mechanistic complexity of the multi-enzyme cellulosome complex
journal, June 2017

Long-term acid-induced wall extension in an in-vitro system
journal, March 1987

Physicochemical Characteristics of Onion ( Allium cepa L.) Tissues
journal, November 2000

Nanoscale movements of cellulose microfibrils in primary cell walls
journal, April 2017

Measuring the mechanics of morphogenesis
journal, February 2013

Colorimetric Method for Determination of Sugars and Related Substances
journal, March 1956

Mode of Action of Exo- and Endo-Type Cellulases from Irpex lacteus in the Hydrolysis of Cellulose with Different Crystallinities
journal, August 1993

Restricted access of proteins to mannan polysaccharides in intact plant cell walls: Masking of mannan polysaccharides
journal, August 2010

Electron Tomography of Cryo-Immobilized Plant Tissue: A Novel Approach to Studying 3D Macromolecular Architecture of Mature Plant Cell Walls In Situ
journal, September 2014

A synthetic biology approach for evaluating the functional contribution of designer cellulosome components to deconstruction of cellulosic substrates
journal, January 2013

Nanoscale structure, mechanics and growth of epidermal cell walls
journal, December 2018

The Growing Outer Epidermal Wall: Design and Physiological Role of a Composite Structure
journal, February 2008

Dual-axis electron tomography: a new approach for investigating the spatial organization of wood cellulose microfibrils
journal, July 2006

Cellular Force Microscopy for in Vivo Measurements of Plant Tissue Mechanics
journal, February 2012

Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls
journal, September 2013

Mechanochemical Polarization of Contiguous Cell Walls Shapes Plant Pavement Cells
journal, November 2017

Changes in Cell Wall Biomechanical Properties in the Xyloglucan-Deficient xxt1/xxt2 Mutant of Arabidopsis
journal, November 2011

Why plants make puzzle cells, and how their shape emerges
journal, February 2018

Architecture-Based Multiscale Computational Modeling of Plant Cell Wall Mechanics to Examine the Hydrogen-Bonding Hypothesis of the Cell Wall Network Structure Model
journal, August 2012

Extensibility of isolated cell walls: Measurement and changes during cell elongation
journal, January 1967

Multiscale stress-strain characterization of onion outer epidermal tissue in wet and dry states
journal, January 2015

Shrinking the hammer: micromechanical approaches to morphogenesis
journal, July 2013

Plant expansins: diversity and interactions with plant cell walls
journal, June 2015

Mechanical characterization of outer epidermal middle lamella of onion under tensile loading
journal, May 2014

Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis
journal, March 2015

Synergism between cucumber α-expansin, fungal endoglucanase and pectin lyase
journal, September 2010

Differential Regulation of Cellulose Orientation at the Inner and Outer Face of Epidermal Cells in the Arabidopsis Hypocotyl
journal, July 2011

Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides
journal, December 2016

3D Electron Tomography of Pretreated Biomass Informs Atomic Modeling of Cellulose Microfibrils
journal, August 2013

On the role of stress anisotropy in the growth of stems
journal, August 2013

TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls
journal, September 2016

An oat coleoptile wall protein that induces wall extension in vitro and that is antigenically related to a similar protein from cucumber hypocotyls
journal, August 1993

Loosening of plant cell walls by expansins
journal, September 2000

Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis Primary Cell Walls: Evidence from Solid-State Nuclear Magnetic Resonance
journal, June 2015

Preparation of Onion Epidermal Cell Walls for Imaging by Atomic Force Microscopy (AFM)
journal, January 2017

Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes
journal, November 2015

WallGen, Software to Construct Layered Cellulose-Hemicellulose Networks and Predict Their Small Deformation Mechanics
journal, December 2009

Disrupting Two Arabidopsis thaliana Xylosyltransferase Genes Results in Plants Deficient in Xyloglucan, a Major Primary Cell Wall Component
journal, June 2008

Effects of mechanical stretching on average orientation of cellulose and pectin in onion epidermis cell wall: A polarized FT-IR study
journal, May 2017

Assessment of In Vitro Binding of Isolated Pectic Domains to Cellulose by Adsorption Isotherms, Electron Microscopy, and X-ray Diffraction Methods
journal, January 2007

On the micro-indentation of plant cells in a tissue context
journal, February 2017

Diffuse Growth of Plant Cell Walls
journal, November 2017

Biomass accessibility analysis using electron tomography
journal, December 2015

A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
journal, May 1976