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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 » 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.« less

Authors:
 [1];  [2];  [2]; ORCiD logo [1]
  1. Pennsylvania State Univ., University Park, PA (United States). Dept. of Biology and Center for Lignocellulose Structure and Formation
  2. Lehigh Univ., Bethlehem, PA (United States). Dept. of Physics
Publication Date:
Research Org.:
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) (SC-22)
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.
Zhang, Tian, Tang, Haosu, Vavylonis, Dimitrios, & Cosgrove, Daniel J. Disentangling loosening from softening: insights into primary cell wall structure. United States. doi:10.1111/tpj.14519.
Zhang, Tian, Tang, Haosu, Vavylonis, Dimitrios, and Cosgrove, Daniel J. Fri . "Disentangling loosening from softening: insights into primary cell wall structure". United States. doi:10.1111/tpj.14519.
@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 = {2019},
month = {8}
}

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