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Title: Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex

Abstract

A six-lobed membrane spanning cellulose synthesis complex (CSC) containing multiple cellulose synthase (CESA) glycosyltransferases mediates cellulose microfibril formation. The number of CESAs in the CSC has been debated for decades in light of changing estimates of the diameter of the smallest microfibril formed from the β-1,4 glucan chains synthesized by one CSC. We obtained more direct evidence through generating improved transmission electron microscopy (TEM) images and image averages of the rosette-type CSC, revealing the frequent triangularity and average cross-sectional area in the plasma membrane of its individual lobes. Trimeric oligomers of two alternative CESA computational models corresponded well with individual lobe geometry. A six-fold assembly of the trimeric computational oligomer had the lowest potential energy per monomer and was consistent with rosette CSC morphology. Negative stain TEM and image averaging showed the triangularity of a recombinant CESA cytosolic domain, consistent with previous modeling of its trimeric nature from small angle scattering (SAXS) data. Six trimeric SAXS models nearly filled the space below an average FF-TEM image of the rosette CSC. In conclusion, the multifaceted data support a rosette CSC with 18 CESAs that mediates the synthesis of a fundamental microfibril composed of 18 glucan chains.

Authors:
 [1];  [2];  [3];  [1];  [3];  [3];  [3];  [4];  [4];  [5];  [6];  [3];  [3]
  1. Pennsylvania State Univ., State College, PA (United States)
  2. North Carolina State Univ., Raleigh, NC (United States); Duke Univ., Durham, NC (United States)
  3. North Carolina State Univ., Raleigh, NC (United States)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  5. Rhode Island College, Providence, RI (United States)
  6. Univ. of Rhode Island, Kingston, RI (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). High Flux Isotope Reactor (HFIR); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS); Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1339409
Grant/Contract Number:  
AC05-00OR22725; SC0001090
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cell wall; computational models; electron microscopy

Citation Formats

Nixon, B. Tracy, Mansouri, Katayoun, Singh, Abhishek, Du, Juan, Davis, Jonathan K., Lee, Jung -Goo, Slabaugh, Erin, Vandavasi, Venu Gopal, O’Neill, Hugh Michael, Roberts, Eric M., Roberts, Alison W., Yingling, Yaroslava G., and Haigler, Candace H. Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex. United States: N. p., 2016. Web. doi:10.1038/srep28696.
Nixon, B. Tracy, Mansouri, Katayoun, Singh, Abhishek, Du, Juan, Davis, Jonathan K., Lee, Jung -Goo, Slabaugh, Erin, Vandavasi, Venu Gopal, O’Neill, Hugh Michael, Roberts, Eric M., Roberts, Alison W., Yingling, Yaroslava G., & Haigler, Candace H. Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex. United States. doi:10.1038/srep28696.
Nixon, B. Tracy, Mansouri, Katayoun, Singh, Abhishek, Du, Juan, Davis, Jonathan K., Lee, Jung -Goo, Slabaugh, Erin, Vandavasi, Venu Gopal, O’Neill, Hugh Michael, Roberts, Eric M., Roberts, Alison W., Yingling, Yaroslava G., and Haigler, Candace H. Mon . "Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex". United States. doi:10.1038/srep28696. https://www.osti.gov/servlets/purl/1339409.
@article{osti_1339409,
title = {Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex},
author = {Nixon, B. Tracy and Mansouri, Katayoun and Singh, Abhishek and Du, Juan and Davis, Jonathan K. and Lee, Jung -Goo and Slabaugh, Erin and Vandavasi, Venu Gopal and O’Neill, Hugh Michael and Roberts, Eric M. and Roberts, Alison W. and Yingling, Yaroslava G. and Haigler, Candace H.},
abstractNote = {A six-lobed membrane spanning cellulose synthesis complex (CSC) containing multiple cellulose synthase (CESA) glycosyltransferases mediates cellulose microfibril formation. The number of CESAs in the CSC has been debated for decades in light of changing estimates of the diameter of the smallest microfibril formed from the β-1,4 glucan chains synthesized by one CSC. We obtained more direct evidence through generating improved transmission electron microscopy (TEM) images and image averages of the rosette-type CSC, revealing the frequent triangularity and average cross-sectional area in the plasma membrane of its individual lobes. Trimeric oligomers of two alternative CESA computational models corresponded well with individual lobe geometry. A six-fold assembly of the trimeric computational oligomer had the lowest potential energy per monomer and was consistent with rosette CSC morphology. Negative stain TEM and image averaging showed the triangularity of a recombinant CESA cytosolic domain, consistent with previous modeling of its trimeric nature from small angle scattering (SAXS) data. Six trimeric SAXS models nearly filled the space below an average FF-TEM image of the rosette CSC. In conclusion, the multifaceted data support a rosette CSC with 18 CESAs that mediates the synthesis of a fundamental microfibril composed of 18 glucan chains.},
doi = {10.1038/srep28696},
journal = {Scientific Reports},
issn = {2045-2322},
number = ,
volume = 6,
place = {United States},
year = {2016},
month = {6}
}

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Cited by: 12 works
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Works referenced in this record:

ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers
journal, February 2014


Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls
journal, September 2015

  • Wang, Tuo; Hong, Mei
  • Journal of Experimental Botany, Vol. 67, Issue 2
  • DOI: 10.1093/jxb/erv416

Uniqueness of ab initio shape determination in small-angle scattering
journal, April 2003

  • Volkov, Vladimir V.; Svergun, Dmitri I.
  • Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864
  • DOI: 10.1107/S0021889803000268

Moss cell walls: structure and biosynthesis
journal, January 2012

  • Roberts, Alison W.; Roberts, Eric M.; Haigler, Candace H.
  • Frontiers in Plant Science, Vol. 3
  • DOI: 10.3389/fpls.2012.00166

PatchDock and SymmDock: servers for rigid and symmetric docking
journal, July 2005

  • Schneidman-Duhovny, D.; Inbar, Y.; Nussinov, R.
  • Nucleic Acids Research, Vol. 33, Issue Web Server
  • DOI: 10.1093/nar/gki481

Crystallographic snapshot of cellulose synthesis and membrane translocation
journal, December 2012

  • Morgan, Jacob L. W.; Strumillo, Joanna; Zimmer, Jochen
  • Nature, Vol. 493, Issue 7431
  • DOI: 10.1038/nature11744

Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP
journal, April 2014

  • Morgan, Jacob L. W.; McNamara, Joshua T.; Zimmer, Jochen
  • Nature Structural & Molecular Biology, Vol. 21, Issue 5
  • DOI: 10.1038/nsmb.2803

Prediction of the structures of the plant-specific regions of vascular plant cellulose synthases and correlated functional analysis
journal, October 2015


The plasma membrane of the Funaria caulonema tip cell: morphology and distribution of particle rosettes, and the kinetics of cellulose synthesis
journal, April 1984

  • Reiss, Hans-Dieter; Schnepf, Eberhard; Herth, Werner
  • Planta, Vol. 160, Issue 5
  • DOI: 10.1007/BF00429759

Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes
journal, March 1977

  • Ryckaert, Jean-Paul; Ciccotti, Giovanni; Berendsen, Herman J. C.
  • Journal of Computational Physics, Vol. 23, Issue 3
  • DOI: 10.1016/0021-9991(77)90098-5

Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants
journal, February 1980


Comparison of simple potential functions for simulating liquid water
journal, July 1983

  • Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
  • The Journal of Chemical Physics, Vol. 79, Issue 2
  • DOI: 10.1063/1.445869

Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald
journal, August 2013

  • Salomon-Ferrer, Romelia; Götz, Andreas W.; Poole, Duncan
  • Journal of Chemical Theory and Computation, Vol. 9, Issue 9
  • DOI: 10.1021/ct400314y

A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers
journal, November 2015

  • Vandavasi, Venu Gopal; Putnam, Daniel K.; Zhang, Qiu
  • Plant Physiology, Vol. 170, Issue 1
  • DOI: 10.1104/pp.15.01356

The Structure of the Catalytic Domain of a Plant Cellulose Synthase and Its Assembly into Dimers
journal, July 2014


Structure of Cellulose Microfibrils in Primary Cell Walls from Collenchyma
journal, November 2012

  • Thomas, Lynne H.; Forsyth, V. Trevor; Šturcová, Adriana
  • Plant Physiology, Vol. 161, Issue 1
  • DOI: 10.1104/pp.112.206359

Tertiary model of a plant cellulose synthase
journal, April 2013

  • Sethaphong, L.; Haigler, C. H.; Kubicki, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 18
  • DOI: 10.1073/pnas.1301027110

Comparison of multiple Amber force fields and development of improved protein backbone parameters
journal, November 2006

  • Hornak, Viktor; Abel, Robert; Okur, Asim
  • Proteins: Structure, Function, and Bioinformatics, Vol. 65, Issue 3
  • DOI: 10.1002/prot.21123

Polymorphism of Cellulose I Family:  Reinvestigation of Cellulose IV I
journal, July 2004

  • Wada, Masahisa; Heux, Laurent; Sugiyama, Junji
  • Biomacromolecules, Vol. 5, Issue 4
  • DOI: 10.1021/bm0345357

Nanostructure of cellulose microfibrils in spruce wood
journal, November 2011

  • Fernandes, A. N.; Thomas, L. H.; Altaner, C. M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 47
  • DOI: 10.1073/pnas.1108942108

Catalytic Subunit Stoichiometry within the Cellulose Synthase Complex
journal, October 2014

  • Gonneau, Martine; Desprez, Thierry; Guillot, Alain
  • Plant Physiology, Vol. 166, Issue 4
  • DOI: 10.1104/pp.114.250159

Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase.
journal, October 1996

  • Pear, J. R.; Kawagoe, Y.; Schreckengost, W. E.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 22
  • DOI: 10.1073/pnas.93.22.12637

Molecular Modeling and Imaging of Initial Stages of Cellulose Fibril Assembly: Evidence for a Disordered Intermediate Stage
journal, April 2014


Determination of Domain Structure of Proteins from X-Ray Solution Scattering
journal, June 2001


LIPID11: A Modular Framework for Lipid Simulations Using Amber
journal, August 2012

  • Skjevik, Åge A.; Madej, Benjamin D.; Walker, Ross C.
  • The Journal of Physical Chemistry B, Vol. 116, Issue 36
  • DOI: 10.1021/jp3059992

The Cellulase KORRIGAN Is Part of the Cellulose Synthase Complex
journal, June 2014

  • Vain, Thomas; Crowell, Elizabeth Faris; Timpano, Hélène
  • Plant Physiology, Vol. 165, Issue 4
  • DOI: 10.1104/pp.114.241216

Unique Aspects of the Structure and Dynamics of Elementary I β Cellulose Microfibrils Revealed by Computational Simulations
journal, March 2015

  • Oehme, Daniel P.; Downton, Matthew T.; Doblin, Monika S.
  • Plant Physiology, Vol. 168, Issue 1
  • DOI: 10.1104/pp.114.254664

EMAN2: An extensible image processing suite for electron microscopy
journal, January 2007

  • Tang, Guang; Peng, Liwei; Baldwin, Philip R.
  • Journal of Structural Biology, Vol. 157, Issue 1
  • DOI: 10.1016/j.jsb.2006.05.009

Geometry-based flexible and symmetric protein docking
journal, June 2005

  • Schneidman-Duhovny, Dina; Inbar, Yuval; Nussinov, Ruth
  • Proteins: Structure, Function, and Bioinformatics, Vol. 60, Issue 2
  • DOI: 10.1002/prot.20562

A Bayesian View on Cryo-EM Structure Determination
journal, January 2012


Immunogold Labeling of Rosette Terminal Cellulose-Synthesizing Complexes in the Vascular Plant Vigna angularis
journal, November 1999

  • Kimura, Satoshi; Laosinchai, Walairat; Itoh, Takao
  • The Plant Cell, Vol. 11, Issue 11
  • DOI: 10.1105/tpc.11.11.2075

Molecular dynamics with coupling to an external bath
journal, October 1984

  • Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.
  • The Journal of Chemical Physics, Vol. 81, Issue 8
  • DOI: 10.1063/1.448118

Crystallographic aspects of sub-elementary cellulose fibrils occurring in the wall of rose cells culturedin vitro
journal, September 1979

  • Chanzy, H.; Imada, K.; Mollard, A.
  • Protoplasma, Vol. 100, Issue 3-4
  • DOI: 10.1007/BF01279318

A Mechanism for Sustained Cellulose Synthesis during Salt Stress
journal, September 2015


Freeze-etching nomenclature
journal, October 1975


The cytoplasmic domain of the cellulose-synthesizing complex in vascular plants
journal, August 2008


Automated matching of high- and low-resolution structural models
journal, February 2001


Electron diffraction from the primary wall of cotton fibers
journal, September 1978

  • Chanzy, H.; Imada, K.; Vuong, R.
  • Protoplasma, Vol. 94, Issue 3-4
  • DOI: 10.1007/BF01276778

The Arabidopsis Cellulose Synthase Complex: A Proposed Hexamer of CESA Trimers in an Equimolar Stoichiometry
journal, December 2014

  • Hill, Joseph L.; Hammudi, Mustafa B.; Tien, Ming
  • The Plant Cell, Vol. 26, Issue 12
  • DOI: 10.1105/tpc.114.131193

A smooth particle mesh Ewald method
journal, November 1995

  • Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L.
  • The Journal of Chemical Physics, Vol. 103, Issue 19
  • DOI: 10.1063/1.470117

Cellulose synthases: new insights from crystallography and modeling
journal, February 2014


VMD: Visual molecular dynamics
journal, February 1996


The Cellulose Synthase Complex: A Polymerization Driven Supramolecular Motor
journal, April 2007


Using Sculptor and Situs for simultaneous assembly of atomic components into low-resolution shapes
journal, March 2011

  • Birmanns, Stefan; Rusu, Mirabela; Wriggers, Willy
  • Journal of Structural Biology, Vol. 173, Issue 3
  • DOI: 10.1016/j.jsb.2010.11.002

    Works referencing / citing this record:

    Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants
    journal, May 2019

    • Li, Xingxing; Speicher, Tori L.; Dees, Dianka C. T.
    • The Plant Journal
    • DOI: 10.1111/tpj.14366

    Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants
    journal, May 2019

    • Li, Xingxing; Speicher, Tori L.; Dees, Dianka C. T.
    • The Plant Journal
    • DOI: 10.1111/tpj.14366

    Identifying Stable Fragments of Arabidopsis thaliana Cellulose Synthase Subunit 3 by Yeast Display
    journal, September 2018

    • Raeeszadeh‐Sarmazdeh, Maryam; Patel, Nikhil; Cruise, Sarah
    • Biotechnology Journal, Vol. 14, Issue 4
    • DOI: 10.1002/biot.201800353

    Investigation of stability of branched structures in softwood cellulose using SEC/MALLS/RI/UV and sugar composition analyses
    journal, February 2018


    An evaluation of the structures of cellulose generated by the CHARMM force field: comparisons to in planta cellulose
    journal, April 2018


    Probing cellulose structures with vibrational spectroscopy
    journal, January 2019


    Chirality and bound water in the hierarchical cellulose structure
    journal, June 2019


    Functional divergence of cellulose synthase orthologs in between wild Gossypium raimondii and domesticated G. arboreum diploid cotton species
    journal, September 2019


    The Shape of Native Plant Cellulose Microfibrils
    journal, September 2018


    Optimization of nucleotide sugar supply for polysaccharide formation via thermodynamic buffering
    journal, January 2020

    • Kleczkowski, Leszek A.; Igamberdiev, Abir U.
    • Biochemical Journal, Vol. 477, Issue 2
    • DOI: 10.1042/bcj20190807

    Cellulosic fibres of flax recruit both primary and secondary cell wall cellulose synthases during deposition of thick tertiary cell walls and in the course of graviresponse
    journal, January 2017

    • Mokshina, Natalia; Gorshkov, Oleg; Ibragimova, Nadezda
    • Functional Plant Biology, Vol. 44, Issue 8
    • DOI: 10.1071/fp17105

    Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation
    journal, June 2018

    • Watanabe, Yoichiro; Schneider, Rene; Barkwill, Sarah
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 27
    • DOI: 10.1073/pnas.1802113115

    The cell biology of secondary cell wall biosynthesis
    journal, February 2018

    • Meents, Miranda J.; Watanabe, Yoichiro; Samuels, A. Lacey
    • Annals of Botany, Vol. 121, Issue 6
    • DOI: 10.1093/aob/mcy005

    Structure of native cellulose microfibrils, the starting point for nanocellulose manufacture
    journal, December 2017

    • Jarvis, Michael C.
    • Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 376, Issue 2112
    • DOI: 10.1098/rsta.2017.0045

    Cellulose synthase complex organization and cellulose microfibril structure
    journal, December 2017

    • Turner, Simon; Kumar, Manoj
    • Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 376, Issue 2112
    • DOI: 10.1098/rsta.2017.0048

    Secondary cell wall biosynthesis
    journal, November 2018

    • Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng‐Hua
    • New Phytologist, Vol. 221, Issue 4
    • DOI: 10.1111/nph.15537

    Heterologous overexpression, purification and functional analysis of plant cellulose synthase from green bamboo
    journal, July 2019


    Building a plant cell wall at a glance
    journal, January 2018

    • Lampugnani, Edwin R.; Khan, Ghazanfar Abbas; Somssich, Marc
    • Journal of Cell Science, Vol. 131, Issue 2
    • DOI: 10.1242/jcs.207373

    Differences in protein structural regions that impact functional specificity in GT2 family β-glucan synthases
    journal, October 2019


    Progress and Opportunities in the Characterization of Cellulose – An Important Regulator of Cell Wall Growth and Mechanics
    journal, March 2019


    Secondary Wall Regulating NACs Differentially Bind at the Promoter at a CELLULOSE SYNTHASE A4 Cis-eQTL
    journal, December 2018