Molecular insights into the complex mechanics of plant epidermal cell walls (2025)

Science

2021

DOI: 10.1126/science.abf2824

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Yao Zhang

1

,

Jingyi Yu

2

,

Xuan Wang

3

et al.

Abstract: Plants have evolved complex nanofibril-based cell walls to meet diverse biological and physical constraints. How strength and extensibility emerge from the nanoscale-to-mesoscale organization of growing cell walls has long been unresolved. We sought to clarify the mechanical roles of cellulose and matrix polysaccharides by developing a coarse-grained model based on polymer physics that recapitulates aspects of assembly and tensile mechanics of epidermal cell walls. Simple noncovalent binding interactions in th… Show more

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Molecular insights into the complex mechanics of plant epidermal cell walls (5)

Cited by 222 publications

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Molecular insights into the complex mechanics of plant epidermal cell walls (6)

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“…Actually, in the primary cell walls of plants, the lateral interactions between cellulose microfibrils were found to be determinant to mechanical properties as revealed by coarse-grained molecular dynamics simulation. 125 Since the structure of cellulose is known to differ in algae and higher plants, the structural function of cellulose in the organization of algal cell walls requires further assessment by comparing the cellulose-deficient strain with cellulose-rich species.…”

Section: Discussionmentioning

confidence: 99%

Identification and Quantification of Glycans in Whole Cells: Architecture of Microalgal Polysaccharides Described by Solid-State Nuclear Magnetic Resonance

Poulhazan

1

,

Widanage

2

,

Muszyński

3

et al. 2021

J. Am. Chem. Soc.

5234

Microalgae are photosyntheticorganisms widely distributed in natureand serve as a sustainable source of bioproducts. Their carbohydratecomponents are also promising candidates for bioenergy productionand bioremediation, but the structural characterization of these heterogeneouspolymers in cells remains a formidable problem. Here we present awidely applicable protocol for identifying and quantifying the glycancontent using magic-angle-spinning (MAS) solid-state NMR (ssNMR) spectroscopy,with validation from glycosyl linkage and composition analysis deducedfrom mass-spectrometry (MS). Two-dimensional 13C–13C correlation ssNMR spectra of a uniformly 13C-labeledgreen microalga Parachlorella beijerinckii revealthat starch is the most abundant polysaccharide in a naturally cellulose-deficientstrain, and this polymer adopts a well-organized and highly rigidstructure in the cell. Some xyloses are present in both the mobileand rigid domains of the cell wall, with their chemical shifts partiallyaligned with the flat-ribbon 2-fold xylan identified in plants. Surprisingly,most other carbohydrates are largely mobile, regardless of their distributionin glycolipids or cell walls. These structural insights correlatewith the high digestibility of this cellulose-deficient strain, andthe in-cell ssNMR methods will facilitate the investigations of othereconomically important algae species.

“…Actually, in the primary cell walls of plants, the lateral interactions between cellulose microfibrils were found to be determinant to mechanical properties as revealed by coarse-grained molecular dynamics simulation. 125 Since the structure of cellulose is known to differ in algae and higher plants, the structural function of cellulose in the organization of algal cell walls requires further assessment by comparing the cellulose-deficient strain with cellulose-rich species.…”

Section: Discussionmentioning

confidence: 99%

Identification and Quantification of Glycans in Whole Cells: Architecture of Microalgal Polysaccharides Described by Solid-State Nuclear Magnetic Resonance

Poulhazan

1

,

Widanage

2

,

Muszyński

3

et al. 2021

J. Am. Chem. Soc.

5234

Microalgae are photosyntheticorganisms widely distributed in natureand serve as a sustainable source of bioproducts. Their carbohydratecomponents are also promising candidates for bioenergy productionand bioremediation, but the structural characterization of these heterogeneouspolymers in cells remains a formidable problem. Here we present awidely applicable protocol for identifying and quantifying the glycancontent using magic-angle-spinning (MAS) solid-state NMR (ssNMR) spectroscopy,with validation from glycosyl linkage and composition analysis deducedfrom mass-spectrometry (MS). Two-dimensional 13C–13C correlation ssNMR spectra of a uniformly 13C-labeledgreen microalga Parachlorella beijerinckii revealthat starch is the most abundant polysaccharide in a naturally cellulose-deficientstrain, and this polymer adopts a well-organized and highly rigidstructure in the cell. Some xyloses are present in both the mobileand rigid domains of the cell wall, with their chemical shifts partiallyaligned with the flat-ribbon 2-fold xylan identified in plants. Surprisingly,most other carbohydrates are largely mobile, regardless of their distributionin glycolipids or cell walls. These structural insights correlatewith the high digestibility of this cellulose-deficient strain, andthe in-cell ssNMR methods will facilitate the investigations of othereconomically important algae species.

“…The primary cell wall is composed of three distinctive polysaccharides (cellulose, hemicellulose, and pectin) and is usually organized into multilayer nanostructures, especially in the epidermal wall that physically protect and limit growth of leaves and stems [59,60]. In each layer, the cellulose fibrils are arranged in a common direction, forming a reticulated, noncovalent network, but the direction varies between the layers; hemicellulose bind noncovalently to cellulose, and well-hydrated pectins form a gel-like matrix hosting the stiff cellulose network [61]. However, the structure-function of primary plant cell walls is not well understood.…”

Section: Discussionmentioning

confidence: 99%

“…The latest analysis of cell wall models shows that cellulose noncovalently binds together, providing stress-dependent elasticity, stiffening, and then slide over each other as the cell is stretched, thereby providing plasticity. Thus, cellulose is key to the cell wall's strength, rigidity and plasticity [61]. Expansins were discovered in cell walls from cucumber as they responsible for wall extension [62].…”

Section: Discussionmentioning

confidence: 99%

A Gain-of-Function Mutant of IAA7 Inhibits Stem Elongation by Transcriptional Repression of EXPA5 Genes in Brassica napus

Wei

1

,

Zhang

2

,

Zhu

3

et al. 2021

IJMS

153

Plant height is one of the most important agronomic traits of rapeseeds. In this study, we characterized a dwarf Brassica napus mutant, named ndf-2, obtained from fast neutrons and DES mutagenesis. Based on BSA-Seq and genetic properties, we identified causal mutations with a time-saving approach. The ndf-2 mutation was identified on chromosome A03 and can result in an amino acid substitution in the conserved degron motif (GWPPV to EWPPV) of the Auxin/indole-3-acetic acid protein 7 (BnaA03.IAA7) encoded by the causative gene. Aux/IAA protein is one of the core components of the auxin signaling pathway, which regulates many growth and development processes. However, the molecular mechanism of auxin signal regulating plant height is still not well understood. In the following work, we identified that BnaARF6 and BnaARF8 as interactors of BnaA03.IAA7 and BnaEXPA5 as a target of BnaARF6 and BnaARF8. The three genes BnaA03.IAA7, BnaARF6/8 and BnaEXPA5 were highly expressed in stem, suggesting that these genes were involved in stem development. The overexpression of BnaEXPA5 results in larger rosettes leaves and longer inflorescence stems in Arabidopsis thaliana. Our results indicate that BnaA03.IAA7- and BnaARF6/8-dependent auxin signal control stem elongation and plant height by regulating the transcription of BnaEXPA5 gene, which is one of the targets of this signal.

“…A machinery of specific glycosyl transferases, transglycosidases, and hydroxylases generates the diversity in XyG structures, with XyG α-1,6-xyosyltransferases (XXTs) adding αXyl residues, and α-xylosidases (αXYLs) cleaving xyloysl residues from the non-reducing end of XyG cell wall components and XyG oligosaccharides ( Frankova et al , 2013 ; Pauly et al , 2016 ; B. Zhang et al , 2021 ). Interestingly, while XyG-deficient A. thaliana xxt mutants exhibit only minor morphological phenotype changes, xyl1 mutants lacking α-xylosidase enzyme activity exhibit altered XyG side chains, free XyG oligosaccharide accumulation, and specific phenotypic defects during reproduction, seed dispersal, germination, and seedling growth.…”

mentioning

confidence: 99%

“…XyG oligosaccharides were also proposed to directly or indirectly mediate cell wall signalling which can result in altered hormonal biosynthesis or signalling ( Frankova et al , 2013 ; Pauly et al , 2016 ; Sechet et al , 2016 ; Shigeyama et al , 2016 ; B. Zhang et al , 2021 ). The structure of XyG differs between plant species especially in diversity of the side chains; however, despite this, conservation in XyG remodelling mechanisms and enzymes was also established ( Pauly et al , 2016 ; Rubianes et al , 2019 ; Holloway et al , 2021 ).…”

mentioning

confidence: 99%

Xyloglucan remodelling enzymes and the mechanics of plant seed and fruit biology

Steinbrecher

1

,

Leubner‐Metzger

2

2022

Journal of Experimental Botany

65

This article comments on: Di Marzo M, Ebeling Viana V, Banfi C, Cassina V, Corti R, Herrera-Ubaldo H, Babolin N, Guazzotti A, Kiegle E, Gregis V, de Folter S, Sampedro J, Mantegazza F, Colombo L, Ezquer I. 2022. Cell wall modifications by α-XYLOSIDASE1 are required for the control of seed and fruit size. Journal of Experimental Botany 73, 1499–1515.

Molecular insights into the complex mechanics of plant epidermal cell walls (7)

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Molecular insights into the complex mechanics of plant epidermal cell walls (8)

Molecular insights into the complex mechanics of plant epidermal cell walls (2025)

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