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Title: Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated

Abstract

Abstract Cellulose synthases (CESAs) are glycosyltransferases that catalyze formation of cellulose microfibrils in plant cell walls. Seed plant CESA isoforms cluster in six phylogenetic clades, whose non‐interchangeable members play distinct roles within cellulose synthesis complexes (CSCs). A ‘class specific region’ (CSR), with higher sequence similarity within versus between functional CESA classes, has been suggested to contribute to specific activities or interactions of different isoforms. We investigated CESA isoform specificity in the moss, Physcomitrella patens (Hedw.) B. S. G. to gain evolutionary insights into CESA structure/function relationships. Like seed plants, P. patens has oligomeric rosette‐type CSCs, but the PpCESAs diverged independently and form a separate CESA clade. We showed that P. patens has two functionally distinct CESAs classes, based on the ability to complement the gametophore‐negative phenotype of a ppcesa5 knockout line. Thus, non‐interchangeable CESA classes evolved separately in mosses and seed plants. However, testing of chimeric moss CESA genes for complementation demonstrated that functional class‐specificity is not determined by the CSR. Sequence analysis and computational modeling showed that the CSR is intrinsically disordered and contains predicted molecular recognition features, consistent with a possible role in CESA oligomerization and explaining the evolution of class‐specific sequences without selection for class‐specific function.

Authors:
 [1];  [1];  [2];  [2];  [3];  [2];  [3];  [1]
  1. Department of Biological Sciences University of Rhode Island 120 Flagg Road Kingston RI 02881 USA
  2. Department of Materials Science and Engineering North Carolina State University Raleigh NC 27695 USA
  3. Department of Crop and Soil Sciences and Department of Plant and Microbial Biology North Carolina State University Raleigh NC 27695 USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1430743
Grant/Contract Number:  
DE‐SC0001090
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
Journal of Integrative Plant Biology
Additional Journal Information:
Journal Name: Journal of Integrative Plant Biology Journal Volume: 60 Journal Issue: 6; Journal ID: ISSN 1672-9072
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Scavuzzo‐Duggan, Tess R., Chaves, Arielle M., Singh, Abhishek, Sethaphong, Latsavongsakda, Slabaugh, Erin, Yingling, Yaroslava G., Haigler, Candace H., and Roberts, Alison W. Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated. United Kingdom: N. p., 2018. Web. doi:10.1111/jipb.12637.
Scavuzzo‐Duggan, Tess R., Chaves, Arielle M., Singh, Abhishek, Sethaphong, Latsavongsakda, Slabaugh, Erin, Yingling, Yaroslava G., Haigler, Candace H., & Roberts, Alison W. Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated. United Kingdom. https://doi.org/10.1111/jipb.12637
Scavuzzo‐Duggan, Tess R., Chaves, Arielle M., Singh, Abhishek, Sethaphong, Latsavongsakda, Slabaugh, Erin, Yingling, Yaroslava G., Haigler, Candace H., and Roberts, Alison W. Fri . "Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated". United Kingdom. https://doi.org/10.1111/jipb.12637.
@article{osti_1430743,
title = {Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated},
author = {Scavuzzo‐Duggan, Tess R. and Chaves, Arielle M. and Singh, Abhishek and Sethaphong, Latsavongsakda and Slabaugh, Erin and Yingling, Yaroslava G. and Haigler, Candace H. and Roberts, Alison W.},
abstractNote = {Abstract Cellulose synthases (CESAs) are glycosyltransferases that catalyze formation of cellulose microfibrils in plant cell walls. Seed plant CESA isoforms cluster in six phylogenetic clades, whose non‐interchangeable members play distinct roles within cellulose synthesis complexes (CSCs). A ‘class specific region’ (CSR), with higher sequence similarity within versus between functional CESA classes, has been suggested to contribute to specific activities or interactions of different isoforms. We investigated CESA isoform specificity in the moss, Physcomitrella patens (Hedw.) B. S. G. to gain evolutionary insights into CESA structure/function relationships. Like seed plants, P. patens has oligomeric rosette‐type CSCs, but the PpCESAs diverged independently and form a separate CESA clade. We showed that P. patens has two functionally distinct CESAs classes, based on the ability to complement the gametophore‐negative phenotype of a ppcesa5 knockout line. Thus, non‐interchangeable CESA classes evolved separately in mosses and seed plants. However, testing of chimeric moss CESA genes for complementation demonstrated that functional class‐specificity is not determined by the CSR. Sequence analysis and computational modeling showed that the CSR is intrinsically disordered and contains predicted molecular recognition features, consistent with a possible role in CESA oligomerization and explaining the evolution of class‐specific sequences without selection for class‐specific function.},
doi = {10.1111/jipb.12637},
journal = {Journal of Integrative Plant Biology},
number = 6,
volume = 60,
place = {United Kingdom},
year = {Fri Mar 30 00:00:00 EDT 2018},
month = {Fri Mar 30 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/jipb.12637

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Cited by: 18 works
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Works referenced in this record:

A ratchet for protein complexity
journal, January 2012


Moss cell walls: structure and biosynthesis
journal, January 2012

  • Roberts, Alison W.; Roberts, Eric M.; Haigler, Candace H.
  • Frontiers in Plant Science, Vol. 3
  • DOI: 10.3389/fpls.2012.00166

β-D-Glycan synthases and the CesA gene family: lessons to be learned from the mixed-linkage (1→3),(1→4)β-D-glucan synthase
journal, September 2001

  • Vergara, Claudia E.; Carpita, Nicholas C.
  • Plant Molecular Biology, Vol. 47, Issue 1/2, p. 145-160
  • DOI: 10.1023/A:1010631431620

Molecular Analysis of Cellulose Biosynthesis in Arabidopsis
journal, January 1998


The Cell Biology of Cellulose Synthesis
journal, April 2014


PatchDock and SymmDock: servers for rigid and symmetric docking
journal, July 2005

  • Schneidman-Duhovny, D.; Inbar, Y.; Nussinov, R.
  • Nucleic Acids Research, Vol. 33, Issue Web Server
  • DOI: 10.1093/nar/gki481

Crystallographic snapshot of cellulose synthesis and membrane translocation
journal, December 2012

  • Morgan, Jacob L. W.; Strumillo, Joanna; Zimmer, Jochen
  • Nature, Vol. 493, Issue 7431
  • DOI: 10.1038/nature11744

Novel Structural and Functional Motifs in cellulose synthase (CesA) Genes of Bread Wheat (Triticum aestivum, L.)
journal, January 2016


Prediction of the structures of the plant-specific regions of vascular plant cellulose synthases and correlated functional analysis
journal, October 2015


Gaussian Accelerated Molecular Dynamics: Unconstrained Enhanced Sampling and Free Energy Calculation
journal, July 2015

  • Miao, Yinglong; Feher, Victoria A.; McCammon, J. Andrew
  • Journal of Chemical Theory and Computation, Vol. 11, Issue 8
  • DOI: 10.1021/acs.jctc.5b00436

Interactions among three distinct CesA proteins essential for cellulose synthesis
journal, January 2003

  • Taylor, N. G.; Howells, R. M.; Huttly, A. K.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 3
  • DOI: 10.1073/pnas.0337628100

Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants
journal, February 1980


Evolution and disorder
journal, June 2011

  • Brown, Celeste J.; Johnson, Audra K.; Dunker, A. Keith
  • Current Opinion in Structural Biology, Vol. 21, Issue 3
  • DOI: 10.1016/j.sbi.2011.02.005

The Structure of the Catalytic Domain of a Plant Cellulose Synthase and Its Assembly into Dimers
journal, July 2014


A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers
journal, November 2015

  • Vandavasi, Venu Gopal; Putnam, Daniel K.; Zhang, Qiu
  • Plant Physiology, Vol. 170, Issue 1
  • DOI: 10.1104/pp.15.01356

Isolation and characterization of the cellulose synthase genes PpCesA6 and PpCesA7 in Physcomitrella patens
journal, December 2010


Understanding Plant Cellulose Synthases through a Comprehensive Investigation of the Cellulose Synthase Family Sequences
journal, January 2011


An update on the nomenclature for the cellulose synthase genes in Populus
journal, May 2009


Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants
journal, August 2017

  • Norris, Joanna H.; Li, Xingxing; Huang, Shixin
  • Plant Physiology, Vol. 175, Issue 1
  • DOI: 10.1104/pp.17.00885

Tertiary model of a plant cellulose synthase
journal, April 2013

  • Sethaphong, L.; Haigler, C. H.; Kubicki, J. D.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 18
  • DOI: 10.1073/pnas.1301027110

Rice Cellulose SynthaseA8 Plant-Conserved Region Is a Coiled-Coil at the Catalytic Core Entrance
journal, November 2016

  • Rushton, Phillip S.; Olek, Anna T.; Makowski, Lee
  • Plant Physiology, Vol. 173, Issue 1
  • DOI: 10.1104/pp.16.00739

The Cellulose Synthase Gene Superfamily and Biochemical Functions of Xylem-Specific Cellulose Synthase-Like Genes in Populus trichocarpa
journal, September 2006

  • Suzuki, Shiro; Li, Laigeng; Sun, Ying-Hsuan
  • Plant Physiology, Vol. 142, Issue 3
  • DOI: 10.1104/pp.106.086678

A Comparative Analysis of the Plant Cellulose Synthase ( CesA ) Gene Family
journal, August 2000

  • Holland, Neta; Holland, Doron; Helentjaris, Tim
  • Plant Physiology, Vol. 123, Issue 4
  • DOI: 10.1104/pp.123.4.1313

Analysis of Molecular Recognition Features (MoRFs)
journal, October 2006

  • Mohan, Amrita; Oldfield, Christopher J.; Radivojac, Predrag
  • Journal of Molecular Biology, Vol. 362, Issue 5
  • DOI: 10.1016/j.jmb.2006.07.087

Cellulose Synthesis in Higher Plants
journal, November 2006


Characterization of cellulose synthase complexes in Populus xylem differentiation
journal, June 2010


Three Distinct Rice Cellulose Synthase Catalytic Subunit Genes Required for Cellulose Synthesis in the Secondary Wall
journal, August 2003

  • Tanaka, Katsuyuki; Murata, Kazumasa; Yamazaki, Muneo
  • Plant Physiology, Vol. 133, Issue 1
  • DOI: 10.1104/pp.103.022442

Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase.
journal, October 1996

  • Pear, J. R.; Kawagoe, Y.; Schreckengost, W. E.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 22
  • DOI: 10.1073/pnas.93.22.12637

The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens
journal, September 2006


Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis
journal, September 2007

  • Persson, S.; Paredez, A.; Carroll, A.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 39
  • DOI: 10.1073/pnas.0706592104

Intrinsic Disorder and Functional Proteomics
journal, March 2007

  • Radivojac, Predrag; Iakoucheva, Lilia M.; Oldfield, Christopher J.
  • Biophysical Journal, Vol. 92, Issue 5
  • DOI: 10.1529/biophysj.106.094045

The cellulose synthase superfamily in fully sequenced plants and algae
journal, January 2009


Simulating disorder-order transitions in molecular recognition of unstructured proteins: Where folding meets binding
journal, April 2003

  • Verkhivker, G. M.; Bouzida, D.; Gehlhaar, D. K.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 9
  • DOI: 10.1073/pnas.0531373100

Cellulose biosynthesis and deposition in higher plants
journal, April 2008


Protein Structure Prediction Using Rosetta
book, January 2004


A CELLULOSE SYNTHASE (CESA) gene essential for gametophore morphogenesis in the moss Physcomitrella patens
journal, January 2012


Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes
journal, January 2014

  • Zhang, Qisen; Cheetamun, Roshan; Dhugga, Kanwarpal S.
  • BMC Plant Biology, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2229-14-27

A single heterologously expressed plant cellulose synthase isoform is sufficient for cellulose microfibril formation in vitro
journal, September 2016

  • Purushotham, Pallinti; Cho, Sung Hyun; Díaz-Moreno, Sara M.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 40
  • DOI: 10.1073/pnas.1606210113

Perturbation of Brachypodium distachyon CELLULOSE SYNTHASE A4 or 7 results in abnormal cell walls
journal, January 2013

  • Handakumbura, Pubudu P.; Matos, Dominick A.; Osmont, Karen S.
  • BMC Plant Biology, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2229-13-131

Complexes with Mixed Primary and Secondary Cellulose Synthases Are Functional in Arabidopsis Plants
journal, August 2012

  • Carroll, Andrew; Mansoori, Nasim; Li, Shundai
  • Plant Physiology, Vol. 160, Issue 2
  • DOI: 10.1104/pp.112.199208

Probable Inference, the Law of Succession, and Statistical Inference
journal, June 1927


Coupled Folding and Binding with α-Helix-Forming Molecular Recognition Elements
journal, September 2005

  • Oldfield, Christopher J.; Cheng, Yugong; Cortese, Marc S.
  • Biochemistry, Vol. 44, Issue 37
  • DOI: 10.1021/bi050736e

Cellulose synthase gene expression profiling of Physcomitrella patens
journal, December 2015


Immunogold Labeling of Rosette Terminal Cellulose-Synthesizing Complexes in the Vascular Plant Vigna angularis
journal, November 1999

  • Kimura, Satoshi; Laosinchai, Walairat; Itoh, Takao
  • The Plant Cell, Vol. 11, Issue 11
  • DOI: 10.1105/tpc.11.11.2075

A Complementation Assay for in Vivo Protein Structure/Function Analysis in Physcomitrella patens (Funariaceae)
journal, July 2015

  • Scavuzzo-Duggan, Tess R.; Chaves, Arielle M.; Roberts, Alison W.
  • Applications in Plant Sciences, Vol. 3, Issue 7
  • DOI: 10.3732/apps.1500023

PROCUSTE1 Encodes a Cellulose Synthase Required for Normal Cell Elongation Specifically in Roots and Dark-Grown Hypocotyls of Arabidopsis
journal, December 2000

  • Fagard, Mathilde; Desnos, Thierry; Desprez, Thierry
  • The Plant Cell, Vol. 12, Issue 12
  • DOI: 10.1105/tpc.12.12.2409

Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana
journal, September 2007

  • Desprez, T.; Juraniec, M.; Crowell, E. F.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 39
  • DOI: 10.1073/pnas.0706569104

The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution
journal, January 2018

  • Lang, Daniel; Ullrich, Kristian K.; Murat, Florent
  • The Plant Journal, Vol. 93, Issue 3
  • DOI: 10.1111/tpj.13801

Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex
journal, June 2016

  • Nixon, B. Tracy; Mansouri, Katayoun; Singh, Abhishek
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep28696

Fiji: an open-source platform for biological-image analysis
journal, June 2012

  • Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2019

Large-Scale Co-Expression Approach to Dissect Secondary Cell Wall Formation Across Plant Species
journal, January 2011


In vitro demonstration of interactions among zinc-binding domains of cellulose synthases in Arabidopsis and aspen
journal, January 2010

  • Xu, Fuyu; Joshi, Chandrashekhar P.
  • Advances in Bioscience and Biotechnology, Vol. 01, Issue 03
  • DOI: 10.4236/abb.2010.13021

The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes
journal, June 2005


Evolution of increased complexity in a molecular machine
journal, January 2012

  • Finnigan, Gregory C.; Hanson-Smith, Victor; Stevens, Tom H.
  • Nature, Vol. 481, Issue 7381
  • DOI: 10.1038/nature10724

The Glycosyltransferase Repertoire of the Spikemoss Selaginella moellendorffii and a Comparative Study of Its Cell Wall
journal, May 2012


Practically Useful: What the R osetta Protein Modeling Suite Can Do for You
journal, April 2010

  • Kaufmann, Kristian W.; Lemmon, Gordon H.; DeLuca, Samuel L.
  • Biochemistry, Vol. 49, Issue 14
  • DOI: 10.1021/bi902153g

Real-Time Imaging of Cellulose Reorientation during Cell Wall Expansion in Arabidopsis Roots
journal, December 2009

  • Anderson, Charles T.; Carroll, Andrew; Akhmetova, Laila
  • Plant Physiology, Vol. 152, Issue 2
  • DOI: 10.1104/pp.109.150128

The CesA Gene Family of Barley. Quantitative Analysis of Transcripts Reveals Two Groups of Co-Expressed Genes
journal, December 2003

  • Burton, Rachel A.; Shirley, Neil J.; King, Brendon J.
  • Plant Physiology, Vol. 134, Issue 1
  • DOI: 10.1104/pp.103.032904

Protein disorder—a breakthrough invention of evolution?
journal, June 2011

  • Schlessinger, Avner; Schaefer, Christian; Vicedo, Esmeralda
  • Current Opinion in Structural Biology, Vol. 21, Issue 3
  • DOI: 10.1016/j.sbi.2011.03.014

Intrinsically disordered proteins: a 10-year recap
journal, December 2012


Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains
journal, August 2002

  • Kurek, I.; Kawagoe, Y.; Jacob-Wilk, D.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 17
  • DOI: 10.1073/pnas.162077099

Cellulose synthases: new insights from crystallography and modeling
journal, February 2014


Speeding molecular recognition by using the folding funnel: The fly-casting mechanism
journal, July 2000

  • Shoemaker, B. A.; Portman, J. J.; Wolynes, P. G.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 16
  • DOI: 10.1073/pnas.160259697

Functional Analysis of Cellulose Synthase (CESA) Protein Class Specificity
journal, December 2016

  • Kumar, Manoj; Atanassov, Ivan; Turner, Simon
  • Plant Physiology, Vol. 173, Issue 2
  • DOI: 10.1104/pp.16.01642

Local Cues and Asymmetric Cell Divisions Underpin Body Plan Transitions in the Moss Physcomitrella patens
journal, March 2009

  • Harrison, C. Jill; Roeder, Adrienne H. K.; Meyerowitz, Elliot M.
  • Current Biology, Vol. 19, Issue 6
  • DOI: 10.1016/j.cub.2009.02.050