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Title: A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers

Abstract

In cellulose synthesis complex with a “rosette” shape is responsible for synthesis of cellulose chains and their assembly into microfibrils within the cell walls of land plants and their charophyte algal progenitors. The number of cellulose synthase proteins in this large multisubunit transmembrane protein complex and the number of cellulose chains in a microfibril have been debated for many years. This work reports a low resolution structure of the catalytic domain of CESA1 from Arabidopsis (Arabidopsis thaliana; AtCESA1CatD) determined by small-angle scattering techniques and provides the first experimental evidence for the self-assembly of CESA into a stable trimer in solution. The catalytic domain was overexpressed in Escherichia coli, and using a two-step procedure, it was possible to isolate monomeric and trimeric forms of AtCESA1CatD. Furthermore, the conformation of monomeric and trimeric AtCESA1CatD proteins were studied using small-angle neutron scattering and small-angle x-ray scattering. A series of AtCESA1CatD trimer computational models were compared with the small-angle x-ray scattering trimer profile to explore the possible arrangement of the monomers in the trimers. Several candidate trimers were identified with monomers oriented such that the newly synthesized cellulose chains project toward the cell membrane. In these models, the class-specific region is found at themore » periphery of the complex, and the plant-conserved region forms the base of the trimer. Our study strongly supports the “hexamer of trimers” model for the rosette cellulose synthesis complex that synthesizes an 18-chain cellulose microfibril as its fundamental product.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [1];  [1]; ORCiD logo [1];  [3];  [4];  [1];  [1]; ORCiD logo [1];  [5];  [2]; ORCiD logo [6]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Vanderbilt Univ., Nashville, TN (United States)
  3. Pennsylvania State Univ., University Park, PA (United States)
  4. North Carolina State Univ., Raleigh, NC (United States)
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); 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); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Structural Molecular Biology (CSMB)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1261509
Alternate Identifier(s):
OSTI ID: 1326474
Grant/Contract Number:  
AC05-00OR22725; AC02-98CH10886
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Plant Physiology (Bethesda)
Additional Journal Information:
Journal Volume: 170; Journal Issue: 1; Journal ID: ISSN 0032-0889
Publisher:
American Society of Plant Biologists
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Vandavasi, Venu Gopal, Putnam, Daniel K., Zhang, Qiu, Petridis, Loukas, Heller, William T., Nixon, B. Tracy, Haigler, Candace H., Kalluri, Udaya, Coates, Leighton, Langan, Paul, Smith, Jeremy C., Meiler, Jens, and O’Neill, Hugh. A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers. United States: N. p., 2015. Web. doi:10.1104/pp.15.01356.
Vandavasi, Venu Gopal, Putnam, Daniel K., Zhang, Qiu, Petridis, Loukas, Heller, William T., Nixon, B. Tracy, Haigler, Candace H., Kalluri, Udaya, Coates, Leighton, Langan, Paul, Smith, Jeremy C., Meiler, Jens, & O’Neill, Hugh. A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers. United States. doi:10.1104/pp.15.01356.
Vandavasi, Venu Gopal, Putnam, Daniel K., Zhang, Qiu, Petridis, Loukas, Heller, William T., Nixon, B. Tracy, Haigler, Candace H., Kalluri, Udaya, Coates, Leighton, Langan, Paul, Smith, Jeremy C., Meiler, Jens, and O’Neill, Hugh. Tue . "A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers". United States. doi:10.1104/pp.15.01356. https://www.osti.gov/servlets/purl/1261509.
@article{osti_1261509,
title = {A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers},
author = {Vandavasi, Venu Gopal and Putnam, Daniel K. and Zhang, Qiu and Petridis, Loukas and Heller, William T. and Nixon, B. Tracy and Haigler, Candace H. and Kalluri, Udaya and Coates, Leighton and Langan, Paul and Smith, Jeremy C. and Meiler, Jens and O’Neill, Hugh},
abstractNote = {In cellulose synthesis complex with a “rosette” shape is responsible for synthesis of cellulose chains and their assembly into microfibrils within the cell walls of land plants and their charophyte algal progenitors. The number of cellulose synthase proteins in this large multisubunit transmembrane protein complex and the number of cellulose chains in a microfibril have been debated for many years. This work reports a low resolution structure of the catalytic domain of CESA1 from Arabidopsis (Arabidopsis thaliana; AtCESA1CatD) determined by small-angle scattering techniques and provides the first experimental evidence for the self-assembly of CESA into a stable trimer in solution. The catalytic domain was overexpressed in Escherichia coli, and using a two-step procedure, it was possible to isolate monomeric and trimeric forms of AtCESA1CatD. Furthermore, the conformation of monomeric and trimeric AtCESA1CatD proteins were studied using small-angle neutron scattering and small-angle x-ray scattering. A series of AtCESA1CatD trimer computational models were compared with the small-angle x-ray scattering trimer profile to explore the possible arrangement of the monomers in the trimers. Several candidate trimers were identified with monomers oriented such that the newly synthesized cellulose chains project toward the cell membrane. In these models, the class-specific region is found at the periphery of the complex, and the plant-conserved region forms the base of the trimer. Our study strongly supports the “hexamer of trimers” model for the rosette cellulose synthesis complex that synthesizes an 18-chain cellulose microfibril as its fundamental product.},
doi = {10.1104/pp.15.01356},
journal = {Plant Physiology (Bethesda)},
issn = {0032-0889},
number = 1,
volume = 170,
place = {United States},
year = {2015},
month = {11}
}

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