The structure of the catalytic domain of a plant cellulose synthase and its assembly into dimers
Abstract
Cellulose microfibrils are para-crystalline arrays of several dozen linear (1→4)-β-d-glucan chains synthesized at the surface of the cell membrane by large, multimeric complexes of synthase proteins. Recombinant catalytic domains of rice (Oryza sativa) CesA8 cellulose synthase form dimers reversibly as the fundamental scaffold units of architecture in the synthase complex. Specificity of binding to UDP and UDP-Glc indicates a properly folded protein, and binding kinetics indicate that each monomer independently synthesizes single glucan chains of cellulose, i.e., two chains per dimer pair. In contrast to structure modeling predictions, solution x-ray scattering studies demonstrate that the monomer is a two-domain, elongated structure, with the smaller domain coupling two monomers into a dimer. The catalytic core of the monomer is accommodated only near its center, with the plant-specific sequences occupying the small domain and an extension distal to the catalytic domain. This configuration is in stark contrast to the domain organization obtained in predicted structures of plant CesA. As a result, the arrangement of the catalytic domain within the CesA monomer and dimer provides a foundation for constructing structural models of the synthase complex and defining the relationship between the rosette structure and the cellulose microfibrils they synthesize.
- Authors:
-
- Purdue Univ., West Lafayette, IN (United States)
- Northeastern Univ., Boston, MA (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- DeltaG Technologies, San Diego, CA (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1242477
- Report Number(s):
- NREL/JA-2700-63047
Journal ID: ISSN 1040-4651
- Grant/Contract Number:
- AC36-08GO28308
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The Plant Cell
- Additional Journal Information:
- Journal Volume: 26; Journal Issue: 7; Related Information: Plant Cell; Journal ID: ISSN 1040-4651
- Publisher:
- American Society of Plant Biologists
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; plant cellulose synthase; dimer
Citation Formats
Olek, Anna T., Rayon, Catherine, Makowski, Lee, Kim, Hyung Rae, Ciesielski, Peter, Badger, John, Paul, Lake N., Ghosh, Subhangi, Kihara, Daisuke, Crowley, Michael, Himmel, Michael E., Bolin, Jeffrey T., and Carpita, Nicholas C. The structure of the catalytic domain of a plant cellulose synthase and its assembly into dimers. United States: N. p., 2014.
Web. doi:10.1105/tpc.114.126862.
Olek, Anna T., Rayon, Catherine, Makowski, Lee, Kim, Hyung Rae, Ciesielski, Peter, Badger, John, Paul, Lake N., Ghosh, Subhangi, Kihara, Daisuke, Crowley, Michael, Himmel, Michael E., Bolin, Jeffrey T., & Carpita, Nicholas C. The structure of the catalytic domain of a plant cellulose synthase and its assembly into dimers. United States. https://doi.org/10.1105/tpc.114.126862
Olek, Anna T., Rayon, Catherine, Makowski, Lee, Kim, Hyung Rae, Ciesielski, Peter, Badger, John, Paul, Lake N., Ghosh, Subhangi, Kihara, Daisuke, Crowley, Michael, Himmel, Michael E., Bolin, Jeffrey T., and Carpita, Nicholas C. Thu .
"The structure of the catalytic domain of a plant cellulose synthase and its assembly into dimers". United States. https://doi.org/10.1105/tpc.114.126862. https://www.osti.gov/servlets/purl/1242477.
@article{osti_1242477,
title = {The structure of the catalytic domain of a plant cellulose synthase and its assembly into dimers},
author = {Olek, Anna T. and Rayon, Catherine and Makowski, Lee and Kim, Hyung Rae and Ciesielski, Peter and Badger, John and Paul, Lake N. and Ghosh, Subhangi and Kihara, Daisuke and Crowley, Michael and Himmel, Michael E. and Bolin, Jeffrey T. and Carpita, Nicholas C.},
abstractNote = {Cellulose microfibrils are para-crystalline arrays of several dozen linear (1→4)-β-d-glucan chains synthesized at the surface of the cell membrane by large, multimeric complexes of synthase proteins. Recombinant catalytic domains of rice (Oryza sativa) CesA8 cellulose synthase form dimers reversibly as the fundamental scaffold units of architecture in the synthase complex. Specificity of binding to UDP and UDP-Glc indicates a properly folded protein, and binding kinetics indicate that each monomer independently synthesizes single glucan chains of cellulose, i.e., two chains per dimer pair. In contrast to structure modeling predictions, solution x-ray scattering studies demonstrate that the monomer is a two-domain, elongated structure, with the smaller domain coupling two monomers into a dimer. The catalytic core of the monomer is accommodated only near its center, with the plant-specific sequences occupying the small domain and an extension distal to the catalytic domain. This configuration is in stark contrast to the domain organization obtained in predicted structures of plant CesA. As a result, the arrangement of the catalytic domain within the CesA monomer and dimer provides a foundation for constructing structural models of the synthase complex and defining the relationship between the rosette structure and the cellulose microfibrils they synthesize.},
doi = {10.1105/tpc.114.126862},
journal = {The Plant Cell},
number = 7,
volume = 26,
place = {United States},
year = {Thu Jul 10 00:00:00 EDT 2014},
month = {Thu Jul 10 00:00:00 EDT 2014}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 44 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referencing / citing this record:
Lignocellulosic bioma ss : Biosynthesis, degradation, and industrial utilization
journal, October 2015
- Guerriero, Gea; Hausman, Jean-Francois; Strauss, Joseph
- Engineering in Life Sciences, Vol. 16, Issue 1
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
A mutation in the catalytic domain of cellulose synthase 6 halts its transport to the Golgi apparatus
journal, September 2019
- Park, Sungjin; Song, Bo; Shen, Wei
- Journal of Experimental Botany, Vol. 70, Issue 21
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
OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice
journal, March 2017
- Li, Fengcheng; Xie, Guosheng; Huang, Jiangfeng
- Plant Biotechnology Journal, Vol. 15, Issue 9
Membrane pore architecture of the CslF6 protein controls (1-3,1-4)-β-glucan structure
journal, June 2015
- Jobling, Stephen A.
- Science Advances, Vol. 1, Issue 5
Heterologous overexpression, purification and functional analysis of plant cellulose synthase from green bamboo
journal, July 2019
- Huang, Hsuan-Yu; Cheng, Yi-Sheng
- Plant Methods, Vol. 15, Issue 1
A novel FC17/CESA4 mutation causes increased biomass saccharification and lodging resistance by remodeling cell wall in rice
journal, November 2018
- Li, Fengcheng; Liu, Sitong; Xu, Hai
- Biotechnology for Biofuels, Vol. 11, Issue 1
Differences in protein structural regions that impact functional specificity in GT2 family β-glucan synthases
journal, October 2019
- Oehme, Daniel P.; Shafee, Thomas; Downton, Matthew T.
- PLOS ONE, Vol. 14, Issue 10
Differences in protein structural regions that impact functional specificity in GT2 family β- Glucan synthases
text, January 2021
- Oehme, Daniel P.; Shafee, Thomas; Downton, Matthew T.
- La Trobe
Domain swaps of Arabidopsis secondary wall cellulose synthases to elucidate their class specificity
journal, July 2018
- Hill, Joseph Lee; Hill, Ashley Nicole; Roberts, Alison W.
- Plant Direct, Vol. 2, Issue 7
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
Prediction of Local Quality of Protein Structure Models Considering Spatial Neighbors in Graphical Models
journal, January 2017
- Shin, Woong-Hee; Kang, Xuejiao; Zhang, Jian
- Scientific Reports, Vol. 7, Issue 1
Membrane pore architecture of the CslF6 protein controls (1-3,1-4)-β-glucan structure
journal, June 2015
- Jobling, Stephen A.
- Science Advances, Vol. 1, Issue 5
Heterologous overexpression, purification and functional analysis of plant cellulose synthase from green bamboo
journal, July 2019
- Huang, Hsuan-Yu; Cheng, Yi-Sheng
- Plant Methods, Vol. 15, Issue 1
A novel FC17/CESA4 mutation causes increased biomass saccharification and lodging resistance by remodeling cell wall in rice
journal, November 2018
- Li, Fengcheng; Liu, Sitong; Xu, Hai
- Biotechnology for Biofuels, Vol. 11, Issue 1
Differences in protein structural regions that impact functional specificity in GT2 family β-glucan synthases
journal, October 2019
- Oehme, Daniel P.; Shafee, Thomas; Downton, Matthew T.
- PLOS ONE, Vol. 14, Issue 10
Alleles Causing Resistance to Isoxaben and Flupoxam Highlight the Significance of Transmembrane Domains for CESA Protein Function
journal, August 2018
- Shim, Isaac; Law, Robert; Kileeg, Zachary
- Frontiers in Plant Science, Vol. 9