Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls

Crowe, Jacob D.; Hao, Pengchao; Pattathil, Sivakumar; Pan, Henry; Ding, Shi-You; Hodge, David B.; Jensen, Jacob Krüger

doi:10.3389/fpls.2021.737690

Title: Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls

Journal Article · Thu Sep 23 00:00:00 EDT 2021 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2021.737690· OSTI ID:1821776

Crowe, Jacob D.; Hao, Pengchao; Pattathil, Sivakumar; Pan, Henry; Ding, Shi-You; Hodge, David B.; Jensen, Jacob Krüger

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.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States); Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Marie Sklodowska-Curie Actions

Grant/Contract Number:: SC0019072; SC0018409; CBET 1336622; MSCA IF 841703

OSTI ID:: 1821776

Alternate ID(s):: OSTI ID: 1852649

Journal Information:: Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 12; ISSN 1664-462X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

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plant sciences
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Title: Xylan Is Critical for Proper Bundling and Alignment of Cellulose Microfibrils in Plant Secondary Cell Walls

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