Interactions between callose and cellulose revealed through the analysis of biopolymer mixtures

Abou-Saleh, Radwa H.; Hernandez-Gomez, Mercedes C.; Amsbury, Sam; Paniagua, Candelas; Bourdon, Matthieu; Miyashima, Shunsuke; Helariutta, Yrjö; Fuller, Martin; Budtova, Tatiana; Connell, Simon D.; Ries, Michael E.; Benitez‐Alfonso, Yoselin

doi:10.1038/s41467-018-06820-y

Cited by 60 publications

(67 citation statements)

References 65 publications

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“…Our multiscale model proposes that the rigid and flexible interactions between cellulose and hemicelluloses are responsible for the distinct compression and tension behavior, with fundamental implications for the function of secondary plant cell walls. In addition, the results have significance for the preparation of lignocellulosic-based materials with targeted properties, where hemicellulose molecular structure and content can be used to induce orientation of cellulose nanofibres 74 and to alter the ductility of cellulose-derived membranes and hydrogels 75,76 . Indeed, the molecular structure of wood hemicelluloses seems to largely influence the assembly of cellulose microfibrils into higher-ordered structures through both rigid and flexible domains with plasticizing and antiplasticizing properties, which in turn may assist in controlling and tuning the biomechanical properties of the derived materials in tension and compression.…”

Section: Discussionmentioning

confidence: 99%

Wood hemicelluloses exert distinct biomechanical contributions to cellulose fibrillar networks

et al. 2020

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Hemicelluloses, a family of heterogeneous polysaccharides with complex molecular structures, constitute a fundamental component of lignocellulosic biomass. However, the contribution of each hemicellulose type to the mechanical properties of secondary plant cell walls remains elusive. Here we homogeneously incorporate different combinations of extracted and purified hemicelluloses (xylans and glucomannans) from softwood and hardwood species into self-assembled networks during cellulose biosynthesis in a bacterial model, without altering the morphology and the crystallinity of the cellulose bundles. These composite hydrogels can be therefore envisioned as models of secondary plant cell walls prior to lignification. The incorporated hemicelluloses exhibit both a rigid phase having close interactions with cellulose, together with a flexible phase contributing to the multiscale architecture of the bacterial cellulose hydrogels. The wood hemicelluloses exhibit distinct biomechanical contributions, with glucomannans increasing the elastic modulus in compression, and xylans contributing to a dramatic increase of the elongation at break under tension. These diverging effects cannot be explained solely from the nature of their direct interactions with cellulose, but can be related to the distinct molecular structure of wood xylans and mannans, the multiphase architecture of the hydrogels and the aggregative effects amongst hemicellulose-coated fibrils. Our study contributes to understanding the specific roles of wood xylans and glucomannans in the biomechanical integrity of secondary cell walls in tension and compression and has significance for the development of lignocellulosic materials with controlled assembly and tailored mechanical properties.

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Section: Discussionmentioning

confidence: 99%

Wood hemicelluloses exert distinct biomechanical contributions to cellulose fibrillar networks

et al. 2020

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“…The properties of callose as a plasticizer allowing for deformation without breakage as opposed to pure cellulose (26) support its transient accumulation during the transition of a membrane network stage to a fenestrated sheet and a mature cell plate. Furthermore, the potential transient interaction with cellulose may also contribute to a flexible yet strong polymer that supports the maturation of the cell plate (26). Taken together, our model provides a basis for understanding how membrane structures evolve in the presence of a spreading force and will likely shed light in such transitions that occur beyond cytokinesis.…”

Section: Parameter Valuementioning

confidence: 81%

A Biophysical Model for Plant Cell Plate Development

Jawaid

Drakakaki

Sinclair

et al. 2020

Preprint

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Plant cell division involves de novo formation of a 'cell plate' that partitions the cytoplasm of the dividing cell. Cell plate formation is directed by orchestrated delivery of cytokinetic vesicles via the phragmoplast, vesicle fusion, and membrane maturation to the nascent cell wall by the timely deposition of polysaccharides such as callose, cellulose, and crosslinking glycans. In contrast to the role of endomembrane protein regulators the role of polysaccharides, particularly callose, in cell plate development is poorly understood. It has been suggested that the transient accumulation of callose provides an anisotropic spreading force which helps the transition of earlier, membrane-network cell plate stages into a more mature fenestrated sheet stage. Here we present a biophysical model based on the Helfrich free energy for membranes that models this spreading force. We show that proper cell plate development in the model is possible, depending upon the selection of the bending modulus, with a twodimensional spreading force parameter of between 2 − 6 / , an osmotic pressure difference of 2 − 10 , and a range of spontaneous curvature between 0 − 0.04 −1 . With these conditions, we can achieve stable membrane conformations in agreement with observed sizes and morphologies corresponding to intermediate stages of cell plate development. Altogether, our mathematical model predicts that a spreading force generated by callose and/or other polysaccharides, coupled with a concurrent decrease in spontaneous curvature, is vital for the transition of a membrane network to a nearly mature cell plate. Significance StatementPlant cell division features the development of a unique membrane network called the cell plate that matures to a cell wall which separates the two daughter cells. During cell plate development, callose, a β-1-3 glucan polymer, is transiently synthesized at the cell plate only to be replaced by cellulose in mature stages. The role for this transient callose accumulation at the cell plate is unknown. It has been suggested that callose provides mechanical stability, as well as a spreading force that widens and expands tubular and fenestrated cell plate structures to aid the maturation of the cell plate. Chemical inhibition of callose deposition results in the failure of cell plate development supporting this hypothesis. This publication establishes the need for a spreading force in cell plate development using a biophysical model that predicts cell plate development in the presence and the absence of this force. Such models can potentially be used to decipher for the transition/maturation of membrane networks upon the deposition of polysaccharide polymers. Main Text

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“…The occurrence of these responses might depend on the biological context; they might also be temporally and mechanistically related. For example, short term responses to ABA might involve changes in cell wall structure, including callose-cellulose interactions (Abou-Saleh et�al. 2018), leading to immediate changes in PD width, while a more permanent modification in callose synthesis/degradation might be required to maintain PD obstruction for a longer-timeframe.…”

mentioning

confidence: 99%

Interactions between callose and cellulose revealed through the analysis of biopolymer mixtures

Cited by 60 publications

References 65 publications

Wood hemicelluloses exert distinct biomechanical contributions to cellulose fibrillar networks

Wood hemicelluloses exert distinct biomechanical contributions to cellulose fibrillar networks

A Biophysical Model for Plant Cell Plate Development

The Role of Abscisic Acid in the Regulation of Plasmodesmata and Symplastic Intercellular Transport

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