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Title: Biochemical and physiological flexibility accompanies reduced cellulose biosynthesis in Brachypodium cesa1S830N

Abstract

Here, we present a study into the mechanisms of primary cell wall cellulose formation in grasses, using the model cereal grass Brachypodium distachyon. The exon found adjacent to the BdCESA1 glycosyltransferase QXXRW motif was targeted using Targeting Induced Local Lesions in Genomes (TILLING) and sequencing candidate amplicons in multiple parallel reactions (SCAMPRing) leading to the identification of the Bdcesa1S830N allele. Plants carrying this missense mutation exhibited a significant reduction in crystalline cellulose content in tissues that rely on the primary cell wall for biomechanical support. However, Bdcesa1S830N plants failed to exhibit the predicted reduction in plant height. In a mechanism unavailable to eudicotyledons, B. distachyon plants homozygous for the Bdcesa1S830N allele appear to overcome the loss of internode expansion anatomically by increasing the number of nodes along the stem. Stem biomechanics were resultantly compromised in Bdcesa1S830N. The Bdcesa1S830N missense mutation did not interfere with BdCESA1 gene expression. However, molecular dynamic simulations of the CELLULOSE SYNTHASE A (CESA) structure with modelled membrane interactions illustrated that Bdcesa1S830N exhibited structural changes in the translated gene product responsible for reduced cellulose biosynthesis. Molecular dynamic simulations showed that substituting S830N resulted in a stabilizing shift in the flexibility of the class specific region arm ofmore » the core catalytic domain of CESA, revealing the importance of this motion to protein function.« less

Authors:
 [1];  [2];  [1];  [3];  [4];  [5];  [2];  [4];  [6];  [1];
  1. Department of Horticulture, University of Kentucky, Lexington, KY, USA
  2. Department of Materials Science and Engineering, North Carolina State University, Raleigh, NC, USA
  3. Donald Danforth Plant Science Center, St. Louis, MO, USA, KWS Gateway Research Center, St. Louis, MO, USA
  4. Donald Danforth Plant Science Center, St. Louis, MO, USA
  5. Donald Danforth Plant Science Center, St. Louis, MO, USA, Syngenta Japan K.K., Chuo-ku, Tokyo, Japan
  6. Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF); Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); USDA
OSTI Identifier:
1570542
Alternate Identifier(s):
OSTI ID: 1767733; OSTI ID: 1873743
Grant/Contract Number:  
SC0001090
Resource Type:
Published Article
Journal Name:
AoB Plants
Additional Journal Information:
Journal Name: AoB Plants Journal Volume: 11 Journal Issue: 5; Journal ID: ISSN 2041-2851
Publisher:
Oxford University Press; Annals of Botany Company
Country of Publication:
United Kingdom
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); biomechanics; cellular expansion; cellulose; CESA; class-specific region; molecular dynamics

Citation Formats

Brabham, Chad, Singh, Abhishek, Stork, Jozsef, Rong, Ying, Kumar, Indrajit, Kikuchi, Kazuhiro, Yingling, Yaroslava G., Brutnell, Thomas P., Rose, Jocelyn K. C., Debolt, Seth, and Jameson, ed., Paula. Biochemical and physiological flexibility accompanies reduced cellulose biosynthesis in Brachypodium cesa1S830N. United Kingdom: N. p., 2019. Web. doi:10.1093/aobpla/plz041.
Brabham, Chad, Singh, Abhishek, Stork, Jozsef, Rong, Ying, Kumar, Indrajit, Kikuchi, Kazuhiro, Yingling, Yaroslava G., Brutnell, Thomas P., Rose, Jocelyn K. C., Debolt, Seth, & Jameson, ed., Paula. Biochemical and physiological flexibility accompanies reduced cellulose biosynthesis in Brachypodium cesa1S830N. United Kingdom. https://doi.org/10.1093/aobpla/plz041
Brabham, Chad, Singh, Abhishek, Stork, Jozsef, Rong, Ying, Kumar, Indrajit, Kikuchi, Kazuhiro, Yingling, Yaroslava G., Brutnell, Thomas P., Rose, Jocelyn K. C., Debolt, Seth, and Jameson, ed., Paula. Sat . "Biochemical and physiological flexibility accompanies reduced cellulose biosynthesis in Brachypodium cesa1S830N". United Kingdom. https://doi.org/10.1093/aobpla/plz041.
@article{osti_1570542,
title = {Biochemical and physiological flexibility accompanies reduced cellulose biosynthesis in Brachypodium cesa1S830N},
author = {Brabham, Chad and Singh, Abhishek and Stork, Jozsef and Rong, Ying and Kumar, Indrajit and Kikuchi, Kazuhiro and Yingling, Yaroslava G. and Brutnell, Thomas P. and Rose, Jocelyn K. C. and Debolt, Seth and Jameson, ed., Paula},
abstractNote = {Here, we present a study into the mechanisms of primary cell wall cellulose formation in grasses, using the model cereal grass Brachypodium distachyon. The exon found adjacent to the BdCESA1 glycosyltransferase QXXRW motif was targeted using Targeting Induced Local Lesions in Genomes (TILLING) and sequencing candidate amplicons in multiple parallel reactions (SCAMPRing) leading to the identification of the Bdcesa1S830N allele. Plants carrying this missense mutation exhibited a significant reduction in crystalline cellulose content in tissues that rely on the primary cell wall for biomechanical support. However, Bdcesa1S830N plants failed to exhibit the predicted reduction in plant height. In a mechanism unavailable to eudicotyledons, B. distachyon plants homozygous for the Bdcesa1S830N allele appear to overcome the loss of internode expansion anatomically by increasing the number of nodes along the stem. Stem biomechanics were resultantly compromised in Bdcesa1S830N. The Bdcesa1S830N missense mutation did not interfere with BdCESA1 gene expression. However, molecular dynamic simulations of the CELLULOSE SYNTHASE A (CESA) structure with modelled membrane interactions illustrated that Bdcesa1S830N exhibited structural changes in the translated gene product responsible for reduced cellulose biosynthesis. Molecular dynamic simulations showed that substituting S830N resulted in a stabilizing shift in the flexibility of the class specific region arm of the core catalytic domain of CESA, revealing the importance of this motion to protein function.},
doi = {10.1093/aobpla/plz041},
journal = {AoB Plants},
number = 5,
volume = 11,
place = {United Kingdom},
year = {Sat Jul 13 00:00:00 EDT 2019},
month = {Sat Jul 13 00:00:00 EDT 2019}
}

Journal Article:
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https://doi.org/10.1093/aobpla/plz041

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