Evidence for Plant-Conserved Region Mediated Trimeric CESAs in Plant Cellulose Synthase Complexes
Abstract
Higher plants synthesize cellulose using membrane-bound, six-lobed cellulose synthase complexes, each lobe containing trimeric cellulose synthases (CESAs). Although molecular biology reports support heteromeric trimers composed of different isoforms, a homomeric trimer was reported for in vitro studies of the catalytic domain of CESA1 of Arabidopsis (AtCESA1CatD) and confirmed in cryoEM structures of full-length CESA8 and CESA7 of poplar and cotton, respectively. In both structures, a small portion of the plant-conserved region (P-CR) forms the only contacts between catalytic domains of the monomers. Here, we report inter-subunit lysine-crosslinks that localize to the small P-CR, negative-stain EM structure, and modeling data for homotrimers of AtCESA1CatD. Molecular dynamics simulations for AtCESA1CatD trimers based on the CESA8 cryoEM structure were stable and dependent upon a small set of residue contacts. The results suggest that homomeric CESA trimers may be important for the synthesis of primary and secondary cell walls and identify key residues for future mutagenic studies.
- Authors:
-
- Sichuan Univ., Chengdu (China); Pennsylvania State Univ., University Park, PA (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Rockefeller Univ., New York, NY (United States)
- Pennsylvania State Univ., University Park, PA (United States)
- North Carolina State Univ., Raleigh, NC (United States)
- Publication Date:
- Research Org.:
- Pennsylvania State Univ., University Park, PA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
- OSTI Identifier:
- 1922484
- Grant/Contract Number:
- SC0001090; P41 GM109824; P41 GM103314
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biomacromolecules
- Additional Journal Information:
- Journal Volume: 23; Journal Issue: 9; Journal ID: ISSN 1525-7797
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; cellulose synthase; cell walls; cryoEM; cellulose synthase complex; structure; plant cell wall; Arabidopsis
Citation Formats
Du, Juan, Vandavasi, Venu Gopal, Molloy, Kelly R., Yang, Hui, Massenburg, Lynnicia N., Singh, Abhishek, Kwansa, Albert L., Yingling, Yaroslava G., O’Neill, Hugh, Chait, Brian T., Kumar, Manish, and Nixon, B. Tracy. Evidence for Plant-Conserved Region Mediated Trimeric CESAs in Plant Cellulose Synthase Complexes. United States: N. p., 2022.
Web. doi:10.1021/acs.biomac.2c00550.
Du, Juan, Vandavasi, Venu Gopal, Molloy, Kelly R., Yang, Hui, Massenburg, Lynnicia N., Singh, Abhishek, Kwansa, Albert L., Yingling, Yaroslava G., O’Neill, Hugh, Chait, Brian T., Kumar, Manish, & Nixon, B. Tracy. Evidence for Plant-Conserved Region Mediated Trimeric CESAs in Plant Cellulose Synthase Complexes. United States. https://doi.org/10.1021/acs.biomac.2c00550
Du, Juan, Vandavasi, Venu Gopal, Molloy, Kelly R., Yang, Hui, Massenburg, Lynnicia N., Singh, Abhishek, Kwansa, Albert L., Yingling, Yaroslava G., O’Neill, Hugh, Chait, Brian T., Kumar, Manish, and Nixon, B. Tracy. Wed .
"Evidence for Plant-Conserved Region Mediated Trimeric CESAs in Plant Cellulose Synthase Complexes". United States. https://doi.org/10.1021/acs.biomac.2c00550. https://www.osti.gov/servlets/purl/1922484.
@article{osti_1922484,
title = {Evidence for Plant-Conserved Region Mediated Trimeric CESAs in Plant Cellulose Synthase Complexes},
author = {Du, Juan and Vandavasi, Venu Gopal and Molloy, Kelly R. and Yang, Hui and Massenburg, Lynnicia N. and Singh, Abhishek and Kwansa, Albert L. and Yingling, Yaroslava G. and O’Neill, Hugh and Chait, Brian T. and Kumar, Manish and Nixon, B. Tracy},
abstractNote = {Higher plants synthesize cellulose using membrane-bound, six-lobed cellulose synthase complexes, each lobe containing trimeric cellulose synthases (CESAs). Although molecular biology reports support heteromeric trimers composed of different isoforms, a homomeric trimer was reported for in vitro studies of the catalytic domain of CESA1 of Arabidopsis (AtCESA1CatD) and confirmed in cryoEM structures of full-length CESA8 and CESA7 of poplar and cotton, respectively. In both structures, a small portion of the plant-conserved region (P-CR) forms the only contacts between catalytic domains of the monomers. Here, we report inter-subunit lysine-crosslinks that localize to the small P-CR, negative-stain EM structure, and modeling data for homotrimers of AtCESA1CatD. Molecular dynamics simulations for AtCESA1CatD trimers based on the CESA8 cryoEM structure were stable and dependent upon a small set of residue contacts. The results suggest that homomeric CESA trimers may be important for the synthesis of primary and secondary cell walls and identify key residues for future mutagenic studies.},
doi = {10.1021/acs.biomac.2c00550},
journal = {Biomacromolecules},
number = 9,
volume = 23,
place = {United States},
year = {Wed Aug 10 00:00:00 EDT 2022},
month = {Wed Aug 10 00:00:00 EDT 2022}
}
Works referenced in this record:
Structural and chemical properties of grass lignocelluloses related to conversion for biofuels
journal, January 2008
- Anderson, William F.; Akin, Danny E.
- Journal of Industrial Microbiology & Biotechnology, Vol. 35, Issue 5
Accurate determination of local defocus and specimen tilt in electron microscopy
journal, June 2003
- Mindell, Joseph A.; Grigorieff, Nikolaus
- Journal of Structural Biology, Vol. 142, Issue 3
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
Cellulose microfibrils: visualization of biosynthetic and orienting complexes in association with the plasma membrane.
journal, January 1976
- Brown, R. M.; Montezinos, D.
- Proceedings of the National Academy of Sciences, Vol. 73, Issue 1
Multiple Cellulose Synthase Catalytic Subunits Are Required for Cellulose Synthesis in Arabidopsis
journal, December 2000
- Taylor, Neil G.; Laurie, Steven; Turner, Simon R.
- The Plant Cell, Vol. 12, Issue 12
Cellulose synthesis complexes are homo-oligomeric and hetero-oligomeric in Physcomitrium patens
journal, January 2022
- Li, Xingxing; Chaves, Arielle M.; Dees, Dianka C. T.
- Plant Physiology, Vol. 188, Issue 4
Architecture of a catalytically active homotrimeric plant cellulose synthase complex
journal, July 2020
- Purushotham, Pallinti; Ho, Ruoya; Zimmer, Jochen
- Science, Vol. 369, Issue 6507
Designing Cell Walls for Improved Bioenergy Production
journal, January 2013
- Nookaraju, Akula; Pandey, Shashank K.; Bae, Hyeun-Jong
- Molecular Plant, Vol. 6, Issue 1
Prediction of the structures of the plant-specific regions of vascular plant cellulose synthases and correlated functional analysis
journal, October 2015
- Sethaphong, Latsavongsakda; Davis, Jonathan K.; Slabaugh, Erin
- Cellulose, Vol. 23, Issue 1
Interactions among three distinct CesA proteins essential for cellulose synthesis
journal, January 2003
- Taylor, N. G.; Howells, R. M.; Huttly, A. K.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 3
Molecular studies of cellulose synthase supercomplex from cotton fiber reveal its unique biochemical properties
journal, April 2022
- Wen, Xingpeng; Zhai, Yufeng; Zhang, Li
- Science China Life Sciences, Vol. 65, Issue 9
Cellulosic Microfibrils: Nascent Stages of Synthesis in a Higher Plant Cell
journal, November 1976
- Mueller, S. C.; Brown, R. M.; Scott, T. K.
- Science, Vol. 194, Issue 4268
Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants
journal, February 1980
- Mueller, S. C.
- The Journal of Cell Biology, Vol. 84, Issue 2
Expression of a Mutant Form of Cellulose Synthase AtCesA7 Causes Dominant Negative Effect on Cellulose Biosynthesis
journal, June 2003
- Zhong, Ruiqin; Morrison, W. Herbert; Freshour, Glenn D.
- Plant Physiology, Vol. 132, Issue 2
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
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
Structural insights into homotrimeric assembly of cellulose synthase CesA7 from Gossypium hirsutum
journal, April 2021
- Zhang, Xiangnan; Xue, Yuan; Guan, Zeyuan
- Plant Biotechnology Journal, Vol. 19, Issue 8
Improved protein structure prediction using predicted interresidue orientations
journal, January 2020
- Yang, Jianyi; Anishchenko, Ivan; Park, Hahnbeom
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 3
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
Rice Cellulose SynthaseA8 Plant-Conserved Region Is a Coiled-Coil at the Catalytic Core Entrance
journal, November 2016
- Rushton, Phillip S.; Olek, Anna T.; Makowski, Lee
- Plant Physiology, Vol. 173, Issue 1
Catalytic Subunit Stoichiometry within the Cellulose Synthase Complex
journal, October 2014
- Gonneau, Martine; Desprez, Thierry; Guillot, Alain
- Plant Physiology, Vol. 166, Issue 4
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
Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis
journal, September 2007
- Persson, S.; Paredez, A.; Carroll, A.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 39
Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls
journal, February 1980
- Giddings, T. H.
- The Journal of Cell Biology, Vol. 84, Issue 2
A single heterologously expressed plant cellulose synthase isoform is sufficient for cellulose microfibril formation in vitro
journal, September 2016
- Purushotham, Pallinti; Cho, Sung Hyun; Díaz-Moreno, Sara M.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 40
Structure of In Vitro-Synthesized Cellulose Fibrils Viewed by Cryo-Electron Tomography and 13C Natural-Abundance Dynamic Nuclear Polarization Solid-State NMR
journal, March 2022
- Deligey, Fabien; Frank, Mark A.; Cho, Sung Hyun
- Biomacromolecules, Vol. 23, Issue 6
Synthesis and Self-Assembly of Cellulose Microfibrils from Reconstituted Cellulose Synthase
journal, August 2017
- Cho, Sung Hyun; Purushotham, Pallinti; Fang, Chao
- Plant Physiology, Vol. 175, Issue 1
The Regulation of Cellulose Biosynthesis in Plants
journal, January 2019
- Polko, Joanna K.; Kieber, Joseph J.
- The Plant Cell, Vol. 31, Issue 2
Optimal Determination of Particle Orientation, Absolute Hand, and Contrast Loss in Single-particle Electron Cryomicroscopy
journal, October 2003
- Rosenthal, Peter B.; Henderson, Richard
- Journal of Molecular Biology, Vol. 333, Issue 4
Elucidating the Mechanisms of Assembly and Subunit Interaction of the Cellulose Synthase Complex of Arabidopsis Secondary Cell Walls
journal, December 2008
- Atanassov, Ivan I.; Pittman, Jon K.; Turner, Simon R.
- Journal of Biological Chemistry, Vol. 284, Issue 6
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
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
Cellulose Synthase Stoichiometry in Aspen Differs from Arabidopsis and Norway Spruce
journal, May 2018
- Zhang, Xueyang; Dominguez, Pia Guadalupe; Kumar, Manoj
- Plant Physiology, Vol. 177, Issue 3
Visualizing density maps with UCSF Chimera
journal, January 2007
- Goddard, Thomas D.; Huang, Conrad C.; Ferrin, Thomas E.
- Journal of Structural Biology, Vol. 157, Issue 1
Iterative Stable Alignment and Clustering of 2D Transmission Electron Microscope Images
journal, February 2012
- Yang, Zhengfan; Fang, Jia; Chittuluru, Johnathan
- Structure, Vol. 20, Issue 2
ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB
journal, July 2015
- Maier, James A.; Martinez, Carmenza; Kasavajhala, Koushik
- Journal of Chemical Theory and Computation, Vol. 11, Issue 8
RELION: Implementation of a Bayesian approach to cryo-EM structure determination
journal, December 2012
- Scheres, Sjors H. W.
- Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530
Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex
journal, June 2016
- Nixon, B. Tracy; Mansouri, Katayoun; Singh, Abhishek
- Scientific Reports, Vol. 6, Issue 1
Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana
journal, September 2007
- Desprez, T.; Juraniec, M.; Crowell, E. F.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 39
Structure of the Cellulose Synthase Complex of Gluconacetobacter hansenii at 23.4 Å Resolution
journal, May 2016
- Du, Juan; Vepachedu, Venkata; Cho, Sung Hyun
- PLOS ONE, Vol. 11, Issue 5
New cellulose synthesizing complexes (terminal complexes) involved in animal cellulose biosynthesis in the tunicateMetandrocarpa uedai
journal, September 1996
- Kimura, S.; Itoh, T.
- Protoplasma, Vol. 194, Issue 3-4
Cell-wall carbohydrates and their modification as a resource for biofuels
journal, May 2008
- Pauly, Markus; Keegstra, Kenneth
- The Plant Journal, Vol. 54, Issue 4, p. 559-568
Wood-Derived Materials for Green Electronics, Biological Devices, and Energy Applications
journal, July 2016
- Zhu, Hongli; Luo, Wei; Ciesielski, Peter N.
- Chemical Reviews, Vol. 116, Issue 16
Cellulose Accumulation and a Cellulose Synthase Gene are Responsible for Cell Aggregation in the Cyanobacterium Thermosynechococcus vulcanus RKN
journal, April 2011
- Kawano, Yusuke; Saotome, Toshiyuki; Ochiai, Yuriko
- Plant and Cell Physiology, Vol. 52, Issue 6
Features of the primary wall CESA complex in wild type and cellulose-deficient mutants of Arabidopsis thaliana
journal, July 2008
- Wang, J.; Elliott, J. E.; Williamson, R. E.
- Journal of Experimental Botany, Vol. 59, Issue 10
SWISS-MODEL: homology modelling of protein structures and complexes
journal, May 2018
- Waterhouse, Andrew; Bertoni, Martino; Bienert, Stefan
- Nucleic Acids Research, Vol. 46, Issue W1
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
Determination of Alkali and Halide Monovalent Ion Parameters for Use in Explicitly Solvated Biomolecular Simulations
journal, July 2008
- Joung, In Suk; Cheatham, Thomas E.
- The Journal of Physical Chemistry B, Vol. 112, Issue 30
In silico structure prediction of full-length cotton cellulose synthase protein (GhCESA1) and its hierarchical complexes
journal, April 2020
- Singh, Abhishek; Kwansa, Albert L.; Kim, Ho Shin
- Cellulose, Vol. 27, Issue 10
Structure of the Bacterial Cellulose Ribbon and Its Assembly-Guiding Cytoskeleton by Electron Cryotomography
journal, January 2021
- Nicolas, William J.; Ghosal, Debnath; Tocheva, Elitza I.
- Journal of Bacteriology, Vol. 203, Issue 3
Structure of Arabidopsis CESA3 catalytic domain with its substrate UDP-glucose provides insight into the mechanism of cellulose synthesis
journal, March 2021
- Qiao, Zhu; Lampugnani, Edwin R.; Yan, Xin-Fu
- Proceedings of the National Academy of Sciences, Vol. 118, Issue 11
Cellulose microfibrils, cell motility, and plasma membrane protein organization change in parallel during culmination in Dictyostelium discoideum
journal, December 1996
- Grimson, M. J.; Haigler, C. H.; Blanton, R. L.
- Journal of Cell Science, Vol. 109, Issue 13
Bacterial Cellulose Production and its Industrial Applications
journal, January 2014
- Keshk, Sherif MAS
- Journal of Bioprocessing & Biotechniques, Vol. 04, Issue 02
Robust evaluation of 3D electron cryomicroscopy data using tilt-pairs
journal, August 2014
- Russo, Christopher J.; Passmore, Lori A.
- Journal of Structural Biology, Vol. 187, Issue 2
Control of Cellulose Synthase Complex Localization in Developing Xylem
journal, July 2003
- Gardiner, John C.; Taylor, Neil G.; Turner, Simon R.
- The Plant Cell, Vol. 15, Issue 8