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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]
+ Show Author Affiliations
  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 Laboratory (ORNL), Oak Ridge, TN (United States). High Flux Isotope Reactor (HFIR); Oak Ridge National Laboratory (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:
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.
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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. https://doi.org/10.1038/srep28696
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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. https://doi.org/10.1038/srep28696. https://www.osti.gov/servlets/purl/1339409.
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@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},
number = ,
volume = 6,
place = {United States},
year = {Mon Jun 27 00:00:00 EDT 2016},
month = {Mon Jun 27 00:00:00 EDT 2016}
}
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