Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

The three cellulose synthase isoforms for secondary cell wall make specific contributions to microfibril synthesis

Journal Article · · The Plant Journal
DOI:https://doi.org/10.1111/tpj.70344· OSTI ID:2575219
 [1];  [1];  [2];  [2];  [1];  [1];  [2];  [3]
  1. The Pennsylvania State University, State College, PA (United States)
  2. Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
  3. University of Massachusetts, Amherst, MA (United States)
Cellulose is synthesized at the plasma membrane by the cellulose synthase complex, a structure that contains three distinct isoforms of the catalytic subunit, cellulose synthase A (CESA). The division into three subunits appears early in land plant evolution and is highly conserved, particularly for the secondary cell wall. However, what if any unique roles each isoform plays in the complex remain unclear. Here, we assessed the contributions of specific isoforms to microfibril synthesis. First, we expressed CESA isoforms of the primary cell wall or the moss Physcomitrium patens in Arabidopsis thaliana backgrounds missing a secondary cell wall CESA. While the primary cell wall isoforms rescued the cesa knockout phenotype with partial isoform specificity, those from the moss rescued with fewer restrictions. Then, we recreated various CESA missense mutations in all three of the secondary cell wall isoforms; while results are consistent with isoform specificity, they are difficult to interpret further without molecular structures. Finally, we show that catalytically inactive CESA isoforms restore growth and cellulose content in the corresponding knockout in an isoform-specific manner; along with partial rescue of the growth and cellulose content of the inflorescence stem, the replacement lines have fiber cells with partially disorganized microfibrils and secondary cell wall cellulose with narrow crystal width. Generally, effects were more pronounced in lines where CESA8 was inactivated compared with inactivating CESA4 or 7, which tended to have similar phenotypes to each other. Here, we account for these results with a model for cellulose synthase structure with the isoforms assigned specific localization within the cellulose synthase complex.
Research Organization:
The Pennsylvania State University, State College, PA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0001090
OSTI ID:
2575219
Journal Information:
The Plant Journal, Journal Name: The Plant Journal Journal Issue: 2 Vol. 123; ISSN 1365-313X; ISSN 0960-7412
Publisher:
Society for Experimental BiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (70)

Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds journal July 2003
Phenotypic effects of changes in the FTVTxK region of an Arabidopsis secondary wall cellulose synthase compared with results from analogous mutations in other isoforms journal August 2021
Domain swaps of Arabidopsis secondary wall cellulose synthases to elucidate their class specificity journal July 2018
Cellulose-Synthesizing Complexes of a Dinoflagellate and other Unique Algae book January 2007
A protocol for rapid DNA extraction fromArabidopsis thaliana for PCR analysis journal March 2004
The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens journal September 2006
Crystallinity and structure of starch using wide angle X-ray scattering journal October 2009
PIN Polarity Maintenance by the Cell Wall in Arabidopsis journal February 2011
Phytochrome Regulation of Cellulose Synthesis in Arabidopsis journal November 2011
Mantid—Data analysis and visualization package for neutron scattering and μ SR experiments
  • Arnold, O.; Bilheux, J. C.; Borreguero, J. M.
  • Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 764 https://doi.org/10.1016/j.nima.2014.07.029
journal November 2014
Smoothing and Differentiation of Data by Simplified Least Squares Procedures. journal July 1964
Evidence for Plant-Conserved Region Mediated Trimeric CESAs in Plant Cellulose Synthase Complexes journal August 2022
Hemicellulose–Cellulose Composites Reveal Differences in Cellulose Organization after Dilute Acid Pretreatment journal December 2018
Understanding Multiscale Structural Changes During Dilute Acid Pretreatment of Switchgrass and Poplar journal December 2016
Breakdown of Cell Wall Nanostructure in Dilute Acid Pretreated Biomass journal September 2010
Crystal Structure and Hydrogen-Bonding System in Cellulose Iβ from Synchrotron X-ray and Neutron Fiber Diffraction journal August 2002
Crystal Structure and Hydrogen Bonding System in Cellulose I α from Synchrotron X-ray and Neutron Fiber Diffraction journal November 2003
Crystallographic snapshot of cellulose synthesis and membrane translocation journal December 2012
NIH Image to ImageJ: 25 years of image analysis journal June 2012
Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex journal June 2016
Root Morphology Mutants in Arabidopsis thaliana journal January 1992
Interactions among three distinct CesA proteins essential for cellulose synthesis journal January 2003
Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis journal September 2007
Nanostructure of cellulose microfibrils in spruce wood journal November 2011
Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1A903V and CESA3T942I of cellulose synthase journal February 2012
Tertiary model of a plant cellulose synthase journal April 2013
A single heterologously expressed plant cellulose synthase isoform is sufficient for cellulose microfibril formation in vitro journal September 2016
Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants journal August 2001
Structure of Arabidopsis CESA3 catalytic domain with its substrate UDP-glucose provides insight into the mechanism of cellulose synthesis journal March 2021
Cellulose microfibrils: visualization of biosynthetic and orienting complexes in association with the plasma membrane. journal January 1976
Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. journal October 1996
Parallel-up structure evidences the molecular directionality during biosynthesis of bacterial cellulose journal August 1997
Computational and genetic evidence that different structural conformations of a non-catalytic region affect the function of plant cellulose synthase journal September 2014
A mutation in the catalytic domain of cellulose synthase 6 halts its transport to the Golgi apparatus journal September 2019
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0 journal April 2007
Multiple sequence alignment with hierarchical clustering journal November 1988
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics journal January 2009
Cellulose synthesis complexes are homo-oligomeric and hetero-oligomeric in Physcomitrium patens journal January 2022
Essential amino acids in the Plant-Conserved and Class-Specific Regions of cellulose synthases journal October 2022
Cellulose synthase complex organization and cellulose microfibril structure journal December 2017
Chimeric Proteins Suggest That the Catalytic and/or C-Terminal Domains Give CesA1 and CesA3 Access to Their Specific Sites in the Cellulose Synthase of Primary Walls journal August 2006
Complexes with Mixed Primary and Secondary Cellulose Synthases Are Functional in Arabidopsis Plants journal August 2012
Structure of Cellulose Microfibrils in Primary Cell Walls from Collenchyma journal November 2012
Wide-Angle X-Ray Scattering and Solid-State Nuclear Magnetic Resonance Data Combined to Test Models for Cellulose Microfibrils in Mung Bean Cell Walls journal October 2013
Catalytic Subunit Stoichiometry within the Cellulose Synthase Complex journal October 2014
The Fragile Fiber1 Kinesin Contributes to Cortical Microtubule-Mediated Trafficking of Cell Wall Components journal February 2015
A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers journal November 2015
Rice Cellulose SynthaseA8 Plant-Conserved Region Is a Coiled-Coil at the Catalytic Core Entrance journal November 2016
Functional Analysis of Cellulose Synthase (CESA) Protein Class Specificity journal December 2016
Gradients in Wall Mechanics and Polysaccharides along Growing Inflorescence Stems journal October 2017
Exploiting CELLULOSE SYNTHASE (CESA) Class Specificity to Probe Cellulose Microfibril Biosynthesis journal March 2018
Cellulose Synthase Stoichiometry in Aspen Differs from Arabidopsis and Norway Spruce journal May 2018
Control of Cellulose Synthase Complex Localization in Developing Xylem journal July 2003
Immunogold Labeling of Rosette Terminal Cellulose-Synthesizing Complexes in the Vascular Plant Vigna angularis journal November 1999
The Structure of the Catalytic Domain of a Plant Cellulose Synthase and Its Assembly into Dimers journal July 2014
The Arabidopsis Cellulose Synthase Complex: A Proposed Hexamer of CESA Trimers in an Equimolar Stoichiometry journal December 2014
Multiple Cellulose Synthase Catalytic Subunits Are Required for Cellulose Synthesis in Arabidopsis journal December 2000
Cellulose Synthesis Takes the CesA Train journal August 2003
Patterned Deposition of Xylan and Lignin is Independent from that of the Secondary Wall Cellulose of Arabidopsis Xylem Vessels journal October 2018
Collapsed Xylem Phenotype of Arabidopsis Identifies Mutants Deficient in Cellulose Deposition in the Secondary Cell Wall journal May 1997
Estimation of the background in powder diffraction patterns through a robust smoothing procedure journal June 2000
Reduction and analysis of SANS and USANS data using IGOR Pro journal November 2006
Irena : tool suite for modeling and analysis of small-angle scattering journal February 2009
Approximations Leading to a Unified Exponential/Power-Law Approach to Small-Angle Scattering journal December 1995
Four alleles of AtCESA3 form an allelic series with respect to root phenotype in Arabidopsis thaliana journal March 2012
Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated: Intrinsic disorder in cellulose synthases journal March 2018
Structural insights into homotrimeric assembly of cellulose synthase CesA7 from Gossypium hirsutum journal April 2021
Molecular Analysis of Cellulose Biosynthesis in Arabidopsis journal January 1998
Architecture of a catalytically active homotrimeric plant cellulose synthase complex journal July 2020
Comprehensive Compositional Analysis of Plant Cell Walls (Lignocellulosic biomass) Part I: Lignin journal January 2010