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Structural Imaging of Native Cryo-Preserved Secondary Cell Walls Reveals the Presence of Macrofibrils and Their Formation Requires Normal Cellulose, Lignin and Xylan Biosynthesis.

Accepted version
Peer-reviewed

Type

Article

Change log

Authors

Lyczakowski, Jan J 
Terrett, Oliver M 
Helariutta, Ykä 

Abstract

The woody secondary cell walls of plants are the largest repository of renewable carbon biopolymers on the planet. These walls are made principally from cellulose and hemicelluloses and are impregnated with lignin. Despite their importance as the main load bearing structure for plant growth, as well as their industrial importance as both a material and energy source, the precise arrangement of these constituents within the cell wall is not yet fully understood. We have adapted low temperature scanning electron microscopy (cryo-SEM) for imaging the nanoscale architecture of angiosperm and gymnosperm cell walls in their native hydrated state. Our work confirms that cell wall macrofibrils, cylindrical structures with a diameter exceeding 10 nm, are a common feature of the native hardwood and softwood samples. We have observed these same structures in Arabidopsis thaliana secondary cell walls, enabling macrofibrils to be compared between mutant lines that are perturbed in cellulose, hemicellulose, and lignin formation. Our analysis indicates that the macrofibrils in Arabidopsis cell walls are dependent upon the proper biosynthesis, or composed, of cellulose, xylan, and lignin. This study establishes that cryo-SEM is a useful additional approach for investigating the native nanoscale architecture and composition of hardwood and softwood secondary cell walls and demonstrates the applicability of Arabidopsis genetic resources to relate fibril structure with wall composition and biosynthesis.

Description

Keywords

cell walls, cellulose, hardwood, lignin, macrofibrils, scanning electron microscopy, softwood, xylan

Journal Title

Front Plant Sci

Conference Name

Journal ISSN

1664-462X
1664-462X

Volume Title

10

Publisher

Frontiers Media SA

Rights

All rights reserved
Sponsorship
Gatsby Charitable Foundation (unknown)
Biotechnology and Biological Sciences Research Council (BB/N013158/1)
European Research Council (323052)
Biotechnology and Biological Sciences Research Council (BB/M015432/1)
Biotechnology and Biological Sciences Research Council (BB/J014540/1)
US Department of Energy (via Pennsylvania State University) (DE-SC0001090)
This work was supported by the Leverhulme Trust Centre for Natural Material Innovation. Analysis of Arabidopsis mutant plants was supported as part of The Center for LignoCellulose Structure and Formation, an Energy Frontier Research Center funded by the U.S. Department of Energy (DOE), Office of Science, Basic Energy Sciences (BES), under Award # DE-SC0001090. JJL was in receipt of a studentship from the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK as part of the Cambridge BBSRC-DTP Programme (Reference BB/J014540/1). JJL is currently supported by a grant from the National Science Centre, Poland as part of the SONATINA 3 programme (project number 2019/32/C/NZ3/00392). MB is employed in YH’s team through the European Research Council Advanced Investigator Grant SYMDEV (No. 323052). YH laboratory is funded by the Finnish Centre of Excellence in Molecular Biology of Primary Producers (Academy of Finland CoE program 2014-2019) (decision #271832); the Gatsby Foundation (GAT3395/PR3); the National Science Foundation Biotechnology and Biological Sciences Research Council grant (BB/N013158/1); University of Helsinki (award 799992091), and the European Research Council Advanced Investigator Grant SYMDEV (No. 323052). OMT was a recipient of an iCASE studentship from the BBSRC (Reference BB/M015432/1). The cryo-SEM facility at the Sainsbury Laboratory is supported by the Gatsby Charitable Foundation