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

Journal Article · Fri Aug 30 00:00:00 EDT 2019 · The Plant Journal

DOI:https://doi.org/10.1111/tpj.14519· OSTI ID:1595717

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

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.

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Research Organization:: 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 Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0001090

OSTI ID:: 1595717

Alternate ID(s):: OSTI ID: 1567708

Journal Information:: The Plant Journal, Vol. 100, Issue 6; ISSN 0960-7412

Publisher:: Society for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 61 works

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Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. Sampathkumar, Arun; Krupinski, Pawel; Wightman, Raymond Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.51507	text	January 2014
Why plants make puzzle cells, and how their shape emerges Sapala, Aleksandra; Runions, Adam; Routier-Kierzkowska, Anne-Lise eLife Sciences Publications Ltd. https://doi.org/10.5167/uzh-165582	text	January 2018
Cellular Force Microscopy for in Vivo Measurements of Plant Tissue Mechanics -L, Routier-Kierzkowska, A.; Weber, A.; Kochova, P. American Society of Plant Biologists https://doi.org/10.5167/uzh-81266	text	January 2012
An automated confocal micro-extensometer enables in vivo quantification of mechanical properties with cellular resolution. Robinson, Sarah Jane; Huflejt, Michal; Barbier De Reuille, Pierre Cold Spring Harbor Laboratory https://doi.org/10.7892/boris.106844	text	January 2017
Anisotropic growth is achieved through the additive mechanical effect of material anisotropy and elastic asymmetry. Bou Daher, Firas; Chen, Yuanjie; Bozorg, Behruz Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.33150	text	January 2018
An automated confocal micro-extensometer enables in vivo quantification of mechanical properties with cellular resolution. Robinson, Sarah; Huflejt, Michal; Barbier De Reuille, Pierre American Society of Plant Biologists https://doi.org/10.7892/boris.107619	text	January 2017

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Combining tensile testing and microscopy to address a diverse range of questions Robinson, Sarah; Durand‐Smet, Pauline Journal of Microscopy, Vol. 278, Issue 3 https://doi.org/10.1111/jmi.12863	journal	February 2020
Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep Wang, Xuan; Wilson, Liza; Cosgrove, Daniel J. Journal of Experimental Botany, Vol. 71, Issue 9 https://doi.org/10.1093/jxb/eraa059	journal	February 2020

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59 BASIC BIOLOGICAL SCIENCES
biomechanics of primary cell walls
atomic force microscopy (AFM)
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cellulose
expansin
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onion (Allium cepa) epidermal cell wall
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Title: Disentangling loosening from softening: insights into primary cell wall structure

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