Disentangling loosening from softening: insights into primary cell wall structure

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

doi:10.1111/tpj.14519

Cited by 89 publications

(120 citation statements)

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“…To assess the effect of HG esterification on cell wall mechanics, outer periclinal walls of onion scale epidermis were prepared as cell-free strips suitable for tensile and indentation assays (Zhang et al , 2019). This pectin-rich wall has a cross-lamellate structure (Zhang et al , 2016), typical of many outer epidermal walls.…”

Section: Resultsmentioning

confidence: 99%

“…The 5th scale, with the 1st being the outermost fleshy scale, was used to make epidermal peels. Abaxial epidermal cells were torn open by peeling 3-mm or 5-mm wide strips midway along the apical-to-basal gradient of the scale, as described previously (Zhang et al , 2014; Zhang et al , 2019). The epidermal peels were washed with 20 mM HEPES (4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid), pH 7.5, with 0.01% (v/v) Tween 20 for 15 min to eliminate the residual cytoplasmic debris, then dipped in boiling methanol for 30 s to deactivate endogenous wall enzymes while retaining α-expansin activity (Cosgrove and Durachko, 1994).…”

Section: Methodsmentioning

confidence: 99%

“…Moreover, the concept of wall stiffness is not as simple as it once seemed, as indentation stiffness (normal to the plane of the cell wall) can vary independently of tensile stiffness (in the plane of the cell wall), e.g. Zhang et al (2019). There is evidence that HG may limit the loosening action of expansins as cells cease growth (Wei et al , 2010; Zhao et al , 2008), but whether this results from wall stiffening or from interference with expansin action by another means is uncertain.…”

Section: Introductionmentioning

confidence: 99%

“…For this study we used the cell-free outer periclinal wall from the onion scale epidermis, because it lends itself to nano-scale indentation and macro-scale tensile tests (Zhang et al , 2019; Zhang et al , 2017). The outer epidermal wall represents a major structural restraint to growth of many organs (Cosgrove, 2018b; Galletti et al , 2016; Kutschera, 1992; Kutschera and Niklas, 2007) and epidermal wall stresses may participate in feedback loops that modulate microtubule patterns and morphogenesis, e.g.…”

Section: Introductionmentioning

confidence: 99%

“…As described elsewhere (Cosgrove, 2018a; Zhang et al , 2019), we make a distinction between wall softening and wall loosening: ‘softening’ makes the wall more deformable to mechanical force (a purely mechanical concept) whereas ‘loosening’ induces wall stress relaxation, leading to irreversible wall enlargement, an essential aspect of cell growth and morphogenesis. Loosening is conveniently measured by creep of a cell wall (slow, irreversible extension that depends on wall modifying agents such as expansin) whereas softening is measured with force/extension assays that assess wall stiffness.…”

Section: Introductionmentioning

confidence: 99%

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Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep

Wang

Cosgrove

2019

Preprint

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De-esterification of homogalacturonan (HG) is thought to stiffen pectin gels and primary cell walls by increasing calcium crosslinking 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.HighlightAfter enzymatic de-esterification without added calcium, the onion epidermal wall swells and becomes softer, as assessed by nanoindentation and tensile plasticity tests, yet exhibits reduced expansin-mediated creep.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep

Wang

Cosgrove

2019

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Plant Cell Growth and Cell Wall Enlargement

Cosgrove¹

2022

Encyclopedia of Life Sciences

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Irreversible cell enlargement begins with cell wall loosening which induces wall stress relaxation, leading to cell water uptake and cell enlargement. Growing cell walls consist of a cohesive network of cellulose microfibrils embedded in hydrophilic pectins and cellulose‐binding hemicelluloses. Models of the growing cell wall are provisional hypotheses about how these wall polymers interact to make a strong yet extensible wall. Recent results clarify how wall strength, plasticity and elasticity depend mostly on the stretching, straightening and sliding of cellulose microfibril networks in the wall. Passive sliding of cellulose microfibrils is facilitated by nonenzymic proteins named expansins while various enzymes modify pectins and hemicelluloses, altering their interactions with each other and with cellulose. Growth cessation is correlated with reduced expression of genes that promote wall loosening as well as changes in the direction of cellulose deposition and the structure of matrix polysaccharides, leading to a less extensible cell wall. Key Concepts Irreversible cell enlargement is an essential aspect of plant growth and morphogenesis. Surface enlargement of the cell wall may be highly localised, as in tip‐growing cells, or more evenly distributed over the cell wall surface, a ‘diffuse growth’ pattern common to most cells in the plant body. Cells typically enlarge substantially after they leave the meristem and before they differentiate into mature cells. Cell growth entails simultaneous uptake of water into the cell and irreversible expansion of the cell wall. In physical terms, growth begins with molecular loosening of the cell wall which leads to wall stress relaxation ; this creates the water potential difference needed for water uptake by the cell, resulting in physical enlargement of the cell. The growing cell wall is composed of a strong noncovalent network of cellulose microfibrils embedded in highly hydrated pectins and hemicelluloses that comprise the soft wall matrix. The tensile (in‐plane) mechanics of growing walls is largely determined by the behaviour of the cellulose microfibril network while pectins influence the indentation (out‐of‐plane) mechanics. Growing plant cell walls typically enlarge more rapidly at low pH (called ‘acid growth’), a process that is mediated by nonenzymatic proteins named α‐expansins; α‐expansins facilitate the passive sliding of a network of cellulose microfibrils in response to tensile wall stresses originating from cell turgor pressure. Deposition of new polymers to the wall is usually coordinated with surface expansion, but these are separable processes. Several classes of enzymes modify the structure of pectins and hemicelluloses in the cell wall, potentially affecting cell wall structure and mechanics. Cell wall mechanical properties are complex, encompassing a number of different physical behaviours that often are not well correlated with each other or with cell wall growth. Cessation of cell enlargement likely involves multiple processes, including changes in the direction of cellulose deposition, stiffening of cellulose and matrix networks, and reduced expression of wall loosening proteins.

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Dynamic Structural Change of Plant Epidermal Cell Walls under Strain

Yu,

Del Mundo,

Freychet

et al. 2024

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The molecular foundations of epidermal cell wall mechanics are critical for understanding structure–function relationships of primary cell walls in plants and facilitating the design of bioinspired materials. To uncover the molecular mechanisms regulating the high extensibility and strength of the cell wall, the onion epidermal wall is stretched uniaxially to various strains and cell wall structures from mesoscale to atomic scale are characterized. Upon longitudinal stretching to high strain, epidermal walls contract in the transverse direction, resulting in a reduced area. Atomic force microscopy shows that cellulose microfibrils exhibit orientation‐dependent rearrangements at high strains: longitudinal microfibrils are straightened out and become highly ordered, while transverse microfibrils curve and kink. Small‐angle X‐ray scattering detects a 7.4 nm spacing aligned along the stretch direction at high strain, which is attributed to distances between individual cellulose microfibrils. Furthermore, wide‐angle X‐ray scattering reveals a widening of (004) lattice spacing and contraction of (200) lattice spacing in longitudinally aligned cellulose microfibrils at high strain, which implies longitudinal stretching of the cellulose crystal. These findings provide molecular insights into the ability of the wall to bear additional load after yielding: the aggregation of longitudinal microfibrils impedes sliding and enables further stretching of the cellulose to bear increased loads.

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Disentangling loosening from softening: insights into primary cell wall structure

Cited by 89 publications

References 101 publications

Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep

Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep

Plant Cell Growth and Cell Wall Enlargement

Dynamic Structural Change of Plant Epidermal Cell Walls under Strain

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