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Title: Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants

Abstract

Cellulose, often touted as the most abundant biopolymer on Earth, is a critical component of the plant cell wall and is synthesized by plasma membrane-spanning cellulose synthase (CESA) enzymes, which in plants are organized into rosette-like CESA complexes (CSCs). Plants construct two types of cell walls, primary cell walls (PCWs) and secondary cell walls (SCWs), which differ in composition, structure, and purpose. Cellulose in PCWs and SCWs is chemically identical but has different physical characteristics. During PCW synthesis, multiple dispersed CSCs move along a shared linear track in opposing directions while synthesizing cellulose microfibrils with low aggregation. In contrast, during SCW synthesis, we observed swaths of densely arranged CSCs that moved in the same direction along tracks while synthesizing cellulose microfibrils that became highly aggregated. Our data support a model in which distinct spatiotemporal features of active CSCs during PCW and SCW synthesis contribute to the formation of cellulose with distinct structure and organization in PCWs and SCWs of Arabidopsis thaliana. In conclusion, this study provides a foundation for understanding differences in the formation, structure, and organization of cellulose in PCWs and SCWs.

Authors:
 [1];  [1];  [2];  [1];  [3];  [4];  [3];  [2];  [1]
  1. Pennsylvania State Univ., University Park, PA (United States). Dept of Biochemistry and Molecular Biology
  2. Pennsylvania State Univ., University Park, PA (United States). Dept of Biology
  3. Pennsylvania State Univ., University Park, PA (United States). Chemical Engineering and Materials Research Inst.
  4. Chinese Academy of Sciences (CAS), Beijing (China). State Key Lab. of Plant Genomics, Inst. of Microbiology
Publication Date:
Research Org.:
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) (SC-22)
OSTI Identifier:
1325833
Alternate Identifier(s):
OSTI ID: 1388836
Grant/Contract Number:  
SC0001090
Resource Type:
Journal Article: Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 40; Related Information: CLSF partners with Pennsylvania State University (lead); North Carolina State University; University of Rhode Island; Virginia Tech University; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biofuels (including algae and biomass); bio-inspired; membrane; carbon sequestration; materials and chemistry by design; synthesis (self-assembly); cellulose synthase complex; live-cell imaging; cellulose microfibrils; plasma membrane; protein dynamics

Citation Formats

Li, Shundai, Bashline, Logan, Zheng, Yunzhen, Xin, Xiaoran, Huang, Shixin, Kong, Zhaosheng, Kim, Seong H., Cosgrove, Daniel J., and Gu, Ying. Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants. United States: N. p., 2016. Web. doi:10.1073/pnas.1613273113.
Li, Shundai, Bashline, Logan, Zheng, Yunzhen, Xin, Xiaoran, Huang, Shixin, Kong, Zhaosheng, Kim, Seong H., Cosgrove, Daniel J., & Gu, Ying. Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants. United States. doi:10.1073/pnas.1613273113.
Li, Shundai, Bashline, Logan, Zheng, Yunzhen, Xin, Xiaoran, Huang, Shixin, Kong, Zhaosheng, Kim, Seong H., Cosgrove, Daniel J., and Gu, Ying. Mon . "Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants". United States. doi:10.1073/pnas.1613273113.
@article{osti_1325833,
title = {Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants},
author = {Li, Shundai and Bashline, Logan and Zheng, Yunzhen and Xin, Xiaoran and Huang, Shixin and Kong, Zhaosheng and Kim, Seong H. and Cosgrove, Daniel J. and Gu, Ying},
abstractNote = {Cellulose, often touted as the most abundant biopolymer on Earth, is a critical component of the plant cell wall and is synthesized by plasma membrane-spanning cellulose synthase (CESA) enzymes, which in plants are organized into rosette-like CESA complexes (CSCs). Plants construct two types of cell walls, primary cell walls (PCWs) and secondary cell walls (SCWs), which differ in composition, structure, and purpose. Cellulose in PCWs and SCWs is chemically identical but has different physical characteristics. During PCW synthesis, multiple dispersed CSCs move along a shared linear track in opposing directions while synthesizing cellulose microfibrils with low aggregation. In contrast, during SCW synthesis, we observed swaths of densely arranged CSCs that moved in the same direction along tracks while synthesizing cellulose microfibrils that became highly aggregated. Our data support a model in which distinct spatiotemporal features of active CSCs during PCW and SCW synthesis contribute to the formation of cellulose with distinct structure and organization in PCWs and SCWs of Arabidopsis thaliana. In conclusion, this study provides a foundation for understanding differences in the formation, structure, and organization of cellulose in PCWs and SCWs.},
doi = {10.1073/pnas.1613273113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 40,
volume = 113,
place = {United States},
year = {Mon Sep 19 00:00:00 EDT 2016},
month = {Mon Sep 19 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1073/pnas.1613273113

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Cited by: 10 works
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Works referenced in this record:

Growth of the plant cell wall
journal, November 2005

  • Cosgrove, Daniel J.
  • Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861
  • DOI: 10.1038/nrm1746