Front Plant Sci. 2021 Sep 23;12:737690. doi: 10.3389/fpls.2021.737690. eCollection 2021.
Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls.
Frontiers in plant science
Jacob D Crowe, Pengchao Hao, Sivakumar Pattathil, Henry Pan, Shi-You Ding, David B Hodge, Jacob Krüger Jensen
Affiliations
Affiliations
- Department of Chemical Engineering & Materials Science, Michigan State University, East Lansing, MI, United States.
- Department of Chemistry, Michigan State University, East Lansing, MI, United States.
- Complex Carbohydrate Research Center, The University of Georgia, Athens, GA, United States.
- Department of Chemical Engineering, University of Texas, Austin, TX, United States.
- Department of Plant Biology, Michigan State University, East Lansing, MI, United States.
- Department of Energy Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, United States.
- Department of Chemical & Biological Engineering, Montana State University, Bozeman, MT, United States.
- Section for Plant Glycobiology, Department of Plant and Environmental Sciences, University of Copenhagen, Copenhagen, Denmark.
PMID: 34630488
PMCID: PMC8495263 DOI: 10.3389/fpls.2021.737690
Abstract
Plant biomass represents an abundant and increasingly important natural resource and it mainly consists of a number of cell types that have undergone extensive secondary cell wall (SCW) formation. These cell types are abundant in the stems of Arabidopsis, a well-studied model system for hardwood, the wood of eudicot plants. The main constituents of hardwood include cellulose, lignin, and xylan, the latter in the form of glucuronoxylan (GX). The binding of GX to cellulose in the eudicot SCW represents one of the best-understood molecular interactions within plant cell walls. The evenly spaced acetylation and 4-O-methyl glucuronic acid (MeGlcA) substitutions of the xylan polymer backbone facilitates binding in a linear two-fold screw conformation to the hydrophilic side of cellulose and signifies a high level of molecular specificity. However, the wider implications of GX-cellulose interactions for cellulose network formation and SCW architecture have remained less explored. In this study, we seek to expand our knowledge on this by characterizing the cellulose microfibril organization in three well-characterized GX mutants. The selected mutants display a range of GX deficiency from mild to severe, with findings indicating even the weakest mutant having significant perturbations of the cellulose network, as visualized by both scanning electron microscopy (SEM) and atomic force microscopy (AFM). We show by image analysis that microfibril width is increased by as much as three times in the severe mutants compared to the wild type and that the degree of directional dispersion of the fibrils is approximately doubled in all the three mutants. Further, we find that these changes correlate with both altered nanomechanical properties of the SCW, as observed by AFM, and with increases in enzymatic hydrolysis. Results from this study indicate the critical role that normal GX composition has on cellulose bundle formation and cellulose organization as a whole within the SCWs.
Copyright © 2021 Crowe, Hao, Pattathil, Pan, Ding, Hodge and Jensen.
Keywords: atomic force micorscopy (AFM); cell wall mechanical properties; cellulose arrangement; cellulose deposition; glucuronoxylan; irregular xylan mutants (irx); secondary cell wall (SCW); xylan (hemicellulose)
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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