skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Structural characterization of a mixed-linkage glucan deficient mutant reveals alteration in cellulose microfibril orientation in rice coleoptile mesophyll cell walls

Abstract

The CELLULOSE SYNTHASE-LIKE F6 (CslF6) gene was previously shown to mediate the biosynthesis of mixed-linkage glucan (MLG), a cell wall polysaccharide that is hypothesized to be tightly associated with cellulose and also have a role in cell expansion in the primary cell wall of young seedlings in grass species. We have recently shown that loss-of-function cslf6 rice mutants do not accumulate MLG in most vegetative tissues. Despite the absence of a structurally important polymer, MLG, these mutants are unexpectedly viable and only show a moderate growth compromise compared to wild type. Therefore these mutants are ideal biological systems to test the current grass cell wall model. In order to gain a better understanding of the role of MLG in the primary wall, we performed in-depth compositional and structural analyses of the cell walls of 3 day-old rice seedlings using various biochemical and novel microspectroscopic approaches. We found that cellulose content as well as matrix polysaccharide composition was not significantly altered in the MLG deficient mutant. However, we observed a significant change in cellulose microfibril bundle organization in mesophyll cell walls of the cslf6 mutant. Using synchrotron source Fourier Transform Mid-Infrared (FTM-IR) Spectromicroscopy for high-resolution imaging, we determined that the bondsmore » associated with cellulose and arabinoxylan, another major component of the primary cell walls of grasses, were in a lower energy configuration compared to wild type, suggesting a slightly weaker primary wall in MLG deficient mesophyll cells. Taken together, these results suggest that MLG may influence cellulose deposition in mesophyll cell walls without significantly affecting anisotropic growth thus challenging MLG importance in cell wall expansion.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [1];  [2];  [3];  [1];  [1];  [1]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of Copenhagen, Copenhagen (Denmark)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Davis, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1257262
Alternate Identifier(s):
OSTI ID: 1512230
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; type II cell walls; cellulose; FT-MIR spectroscopy; mixed-linkage glucan; primary cell wall; rice

Citation Formats

Smith-Moritz, Andreia M., Hao, Zhao, Fernández-Nino, Susana G., Fangel, Jonatan U., Verhertbruggen, Yves, Holman, Hoi-Ying N., Willats, William G. T., Ronald, Pamela C., Scheller, Henrik V., Heazlewood, Joshua L., and Vega-Sanchez, Miguel E. Structural characterization of a mixed-linkage glucan deficient mutant reveals alteration in cellulose microfibril orientation in rice coleoptile mesophyll cell walls. United States: N. p., 2015. Web. https://doi.org/10.3389/fpls.2015.00628.
Smith-Moritz, Andreia M., Hao, Zhao, Fernández-Nino, Susana G., Fangel, Jonatan U., Verhertbruggen, Yves, Holman, Hoi-Ying N., Willats, William G. T., Ronald, Pamela C., Scheller, Henrik V., Heazlewood, Joshua L., & Vega-Sanchez, Miguel E. Structural characterization of a mixed-linkage glucan deficient mutant reveals alteration in cellulose microfibril orientation in rice coleoptile mesophyll cell walls. United States. https://doi.org/10.3389/fpls.2015.00628
Smith-Moritz, Andreia M., Hao, Zhao, Fernández-Nino, Susana G., Fangel, Jonatan U., Verhertbruggen, Yves, Holman, Hoi-Ying N., Willats, William G. T., Ronald, Pamela C., Scheller, Henrik V., Heazlewood, Joshua L., and Vega-Sanchez, Miguel E. Tue . "Structural characterization of a mixed-linkage glucan deficient mutant reveals alteration in cellulose microfibril orientation in rice coleoptile mesophyll cell walls". United States. https://doi.org/10.3389/fpls.2015.00628. https://www.osti.gov/servlets/purl/1257262.
@article{osti_1257262,
title = {Structural characterization of a mixed-linkage glucan deficient mutant reveals alteration in cellulose microfibril orientation in rice coleoptile mesophyll cell walls},
author = {Smith-Moritz, Andreia M. and Hao, Zhao and Fernández-Nino, Susana G. and Fangel, Jonatan U. and Verhertbruggen, Yves and Holman, Hoi-Ying N. and Willats, William G. T. and Ronald, Pamela C. and Scheller, Henrik V. and Heazlewood, Joshua L. and Vega-Sanchez, Miguel E.},
abstractNote = {The CELLULOSE SYNTHASE-LIKE F6 (CslF6) gene was previously shown to mediate the biosynthesis of mixed-linkage glucan (MLG), a cell wall polysaccharide that is hypothesized to be tightly associated with cellulose and also have a role in cell expansion in the primary cell wall of young seedlings in grass species. We have recently shown that loss-of-function cslf6 rice mutants do not accumulate MLG in most vegetative tissues. Despite the absence of a structurally important polymer, MLG, these mutants are unexpectedly viable and only show a moderate growth compromise compared to wild type. Therefore these mutants are ideal biological systems to test the current grass cell wall model. In order to gain a better understanding of the role of MLG in the primary wall, we performed in-depth compositional and structural analyses of the cell walls of 3 day-old rice seedlings using various biochemical and novel microspectroscopic approaches. We found that cellulose content as well as matrix polysaccharide composition was not significantly altered in the MLG deficient mutant. However, we observed a significant change in cellulose microfibril bundle organization in mesophyll cell walls of the cslf6 mutant. Using synchrotron source Fourier Transform Mid-Infrared (FTM-IR) Spectromicroscopy for high-resolution imaging, we determined that the bonds associated with cellulose and arabinoxylan, another major component of the primary cell walls of grasses, were in a lower energy configuration compared to wild type, suggesting a slightly weaker primary wall in MLG deficient mesophyll cells. Taken together, these results suggest that MLG may influence cellulose deposition in mesophyll cell walls without significantly affecting anisotropic growth thus challenging MLG importance in cell wall expansion.},
doi = {10.3389/fpls.2015.00628},
journal = {Frontiers in Plant Science},
number = ,
volume = 6,
place = {United States},
year = {2015},
month = {8}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 4 works
Citation information provided by
Web of Science

Figures / Tables:

FIGURE 1 FIGURE 1: Comprehensive microarray polymer profiling (ComPP) of wild type (NPB) and mutant lines cslf6-1 and cslf6-2. Rice cell wall material was sequentially extracted with CDTA followed by NaOH. The extracts were then subsequently printed on nitrocellulose membranes and probed with a library of cell wall specific monoclonal antibodies tomore » determine relative abundance. In our experiment, the (1–3), (1–4)-$β$-D-glucan antibody labeling (MLG) from NaOH extracted wild type (NPB) samples had the highest fluorescent count and the array was normalized accordingly in reference to the MLG signal. ComPP analysis showed significant difference in only MLG (boxed).« less

Save / Share:

Works referenced in this record:

Virus-Induced Silencing of a Plant Cellulose Synthase Gene
journal, May 2000

  • Burton, Rachel A.; Gibeaut, David M.; Bacic, Antony
  • The Plant Cell, Vol. 12, Issue 5
  • DOI: 10.1105/tpc.12.5.691

(1,3;1,4)-β-D-Glucans in Cell Walls of the Poaceae, Lower Plants, and Fungi: A Tale of Two Linkages
journal, September 2009

  • Burton, Rachel A.; Fincher, Geoffrey B.
  • Molecular Plant, Vol. 2, Issue 5
  • DOI: 10.1093/mp/ssp063

Expansive growth of plant cell walls
journal, January 2000


Cell Wall Architecture of the Elongating Maize Coleoptile
journal, October 2001

  • Carpita, Nicholas C.; Defernez, Marianne; Findlay, Kim
  • Plant Physiology, Vol. 127, Issue 2
  • DOI: 10.1104/Pp.010146

Disrupting Two Arabidopsis thaliana Xylosyltransferase Genes Results in Plants Deficient in Xyloglucan, a Major Primary Cell Wall Component
journal, June 2008

  • Cavalier, David M.; Lerouxel, Olivier; Neumetzler, Lutz
  • The Plant Cell, Vol. 20, Issue 6
  • DOI: 10.1105/tpc.108.059873

A gene from the cellulose synthase-like C family encodes a  -1,4 glucan synthase
journal, May 2007

  • Cocuron, J. -C.; Lerouxel, O.; Drakakaki, G.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 20
  • DOI: 10.1073/pnas.0703133104

Revolutionary Times in Our Understanding of Cell Wall Biosynthesis and Remodeling in the Grasses
journal, January 2009


FT-IR Investigation of Cell Wall Polysaccharides from Cereal Grains. Arabinoxylan Infrared Assignment
journal, September 2005

  • Robert, Paul; Marquis, Mélanie; Barron, Cécile
  • Journal of Agricultural and Food Chemistry, Vol. 53, Issue 18
  • DOI: 10.1021/Jf051145y

Structure and Biogenesis of the cell Walls of Grasses
journal, June 1996


The Structure and Functions of Xyloglucan
journal, January 1989

  • Fry, Stephen C.
  • Journal of Experimental Botany, Vol. 40, Issue 1
  • DOI: 10.1093/jxb/40.1.1

Imaging Cell Wall Architecture in Single Zinnia elegans Tracheary Elements
journal, June 2010

  • Lacayo, Catherine I.; Malkin, Alexander J.; Holman, Hoi-Ying N.
  • Plant Physiology, Vol. 154, Issue 1
  • DOI: 10.1104/pp.110.155242

Understanding the Biological Rationale for the Diversity of Cellulose-directed Carbohydrate-binding Modules in Prokaryotic Enzymes
journal, July 2006

  • Blake, Anthony W.; McCartney, Lesley; Flint, James E.
  • Journal of Biological Chemistry, Vol. 281, Issue 39
  • DOI: 10.1074/jbc.M605903200

Arrangement of mixed-linkage glucan and glucuronoarabinoxylan in the cell walls of growing maize roots
journal, August 2014

  • Kozlova, L. V.; Ageeva, M. V.; Ibragimova, N. N.
  • Annals of Botany, Vol. 114, Issue 6
  • DOI: 10.1093/aob/mcu125

Imaging of colorectal adenocarcinoma using FT-IR microspectroscopy and cluster analysis
journal, March 2004

  • Lasch, Peter; Haensch, Wolfgang; Naumann, Dieter
  • Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1688, Issue 2
  • DOI: 10.1016/j.bbadis.2003.12.006

Changes in Cell Wall Biomechanical Properties in the Xyloglucan-Deficient xxt1/xxt2 Mutant of Arabidopsis
journal, November 2011


Temporal and spatial appearance of wall polysaccharides during cellularization of barley (Hordeum vulgare) endosperm
journal, March 2006


The Rice Oligonucleotide Array Database: an atlas of rice gene expression
journal, January 2012


Brachypodium distachyon grain: characterization of endosperm cell walls
journal, November 2010

  • Guillon, F.; Bouchet, B.; Jamme, F.
  • Journal of Experimental Botany, Vol. 62, Issue 3
  • DOI: 10.1093/Jxb/Erq332

Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes
journal, December 2011

  • Li, S.; Lei, L.; Somerville, C. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 1
  • DOI: 10.1073/pnas.1118560109

Wheat endosperm cell walls: Spatial heterogeneity of polysaccharide structure and composition using micro-scale enzymatic fingerprinting and FT-IR microspectroscopy
journal, November 2009

  • Saulnier, Luc; Robert, Paul; Grintchenko, Mathilde
  • Journal of Cereal Science, Vol. 50, Issue 3
  • DOI: 10.1016/j.jcs.2009.05.003

A simple and rapid method for the permethylation of carbohydrates
journal, August 1984


Cell Wall Development in Maize Coleoptiles
journal, September 1984


Developmental complexity of arabinan polysaccharides and their processing in plant cell walls
journal, August 2009


Thickness and Structure of the Cell Walls in Developing Rye Coleoptiles
journal, November 1994


Spectral pre-processing for biomedical vibrational spectroscopy and microspectroscopic imaging
journal, August 2012


Tensile Properties of Arabidopsis Cell Walls Depend on Both a Xyloglucan Cross-Linked Microfibrillar Network and Rhamnogalacturonan II-Borate Complexes
journal, May 2003

  • Ryden, Peter; Sugimoto-Shirasu, Keiko; Smith, Andrew Charles
  • Plant Physiology, Vol. 132, Issue 2
  • DOI: 10.1104/pp.103.021873

Cell wall polysaccharides from fern leaves: Evidence for a mannan-rich Type III cell wall in Adiantum raddianum
journal, December 2011


Loss of Cellulose Synthase - Like F6 Function Affects Mixed-Linkage Glucan Deposition, Cell Wall Mechanical Properties, and Defense Responses in Vegetative Tissues of Rice
journal, March 2012

  • Vega-Sánchez, Miguel E.; Verhertbruggen, Yves; Christensen, Ulla
  • Plant Physiology, Vol. 159, Issue 1
  • DOI: 10.1104/pp.112.195495

Cellulose orientation determines mechanical anisotropy in onion epidermis cell walls
journal, May 2006


Semimicro determination of cellulose inbiological materials
journal, December 1969


Toward a Systems Approach to Understanding Plant Cell Walls
journal, December 2004


Mixed Linkage (1→3),(1→4)-β- d -Glucans of Grasses
journal, January 2004

  • Buckeridge, Marcos S.; Rayon, Catherine; Urbanowicz, Breeanna
  • Cereal Chemistry Journal, Vol. 81, Issue 1
  • DOI: 10.1094/Cchem.2004.81.1.115

Investigation of macromolecule orientation in dry and hydrated walls of single onion epidermal cells by FTIR microspectroscopy
journal, June 1997


Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles
journal, April 2005


Xyloglucans in the Primary Cell Wall
journal, June 1989


Synchrotron IR Spectromicroscopy: Chemistry of Living Cells
journal, November 2010

  • Holman, Hoi-Ying N.; Bechtel, Hans A.; Hao, Zhao
  • Analytical Chemistry, Vol. 82, Issue 21
  • DOI: 10.1021/Ac100991d

Role of (1,3)(1,4)-β-Glucan in Cell Walls: Interaction with Cellulose
journal, April 2014

  • Kiemle, Sarah N.; Zhang, Xiao; Esker, Alan R.
  • Biomacromolecules, Vol. 15, Issue 5
  • DOI: 10.1021/bm5001247

    Works referencing / citing this record:

    Plant cell wall integrity maintenance in model plants and crop species-relevant cell wall components and underlying guiding principles
    journal, November 2019

    • Gigli-Bisceglia, Nora; Engelsdorf, Timo; Hamann, Thorsten
    • Cellular and Molecular Life Sciences, Vol. 77, Issue 11
    • DOI: 10.1007/s00018-019-03388-8

    The source of inorganic nitrogen has distinct effects on cell wall composition in Brachypodium distachyon
    journal, August 2019

    • Głazowska, Sylwia; Baldwin, Laetitia; Mravec, Jozef
    • Journal of Experimental Botany, Vol. 70, Issue 21
    • DOI: 10.1093/jxb/erz388

    Genetic engineering of grass cell wall polysaccharides for biorefining
    journal, June 2017

    • Bhatia, Rakesh; Gallagher, Joe A.; Gomez, Leonardo D.
    • Plant Biotechnology Journal, Vol. 15, Issue 9
    • DOI: 10.1111/pbi.12764

    In the grass species Brachypodium distachyon , the production of mixed‐linkage (1,3;1,4)‐β‐glucan ( MLG ) occurs in the Golgi apparatus
    journal, February 2018

    • Kim, Sang‐Jin; Zemelis‐Durfee, Starla; Jensen, Jacob Krüger
    • The Plant Journal, Vol. 93, Issue 6
    • DOI: 10.1111/tpj.13830

    The impact of silicon on cell wall composition and enzymatic saccharification of Brachypodium distachyon
    journal, June 2018

    • Głazowska, Sylwia; Baldwin, Laetitia; Mravec, Jozef
    • Biotechnology for Biofuels, Vol. 11, Issue 1
    • DOI: 10.1186/s13068-018-1166-0

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.