Structure/function relationships in the rosette cellulose synthesis complex illuminated by an evolutionary perspective

Haigler, Candace H.; Roberts, Alison W.

doi:10.1007/s10570-018-2157-9

Title: Structure/function relationships in the rosette cellulose synthesis complex illuminated by an evolutionary perspective

Journal Article · Thu Dec 13 00:00:00 EST 2018 · Cellulose

DOI:https://doi.org/10.1007/s10570-018-2157-9· OSTI ID:1595731

Haigler, Candace H. ^[1]; Roberts, Alison W. ^[2]

North Carolina State Univ., Raleigh, NC (United States)
Univ. of Rhode Island, Kingston, RI (United States)

Cellulose microfibrils are a key component of plant cell walls, which in turn compose most of our renewable biomaterials. Consequently, there is considerable interest in understanding how cellulose microfibrils are made in living cells by the plant cellulose synthesis complex (CSC). This remarkable multi-subunit complex contains cellulose synthase (CESA) proteins, and it is often called a rosette due to its six-lobed shape. Each CSC moves within the plasma membrane as it spins a strong cellulose microfibril in its wake. To accomplish this biological manufacturing process, the CESAs harvest an activated sugar substrate from the cytoplasm for use in the polymerization of glucan chains. An elongating glucan is simultaneously translocated across the plasma membrane by each CESA, where the group of chains emanating from one CSC co-crystallizes into a cellulose microfibril that becomes part of the assembling cell wall. Here we review major advances in understanding CESA and CSC structure/function relationships since 2013, when ground-breaking insights about the structure of cellulose synthases in bacteria and plants were published. We additionally discuss: (a) the relationship of CSC substructure to the size of the fundamental cellulose fibril; (b) an evolutionary perspective on the driving force behind the existence of hetero-oligomeric CSCs that currently appear to dominate in land plants; and (c) how cellulose properties may be regulated by CESA and CSC activity. Finally, we also pose major questions that still remain in this rapidly changing and exciting research field.

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Research Organization:: North Carolina State University, Raleigh, NC (United States); Univ. of Rhode Island, Kingston, RI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0001090

OSTI ID:: 1595731

Journal Information:: Cellulose, Vol. 26, Issue 1; ISSN 0969-0239

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 23 works

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References (127)

Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls Wang, Tuo; Hong, Mei Journal of Experimental Botany, Vol. 67, Issue 2 https://doi.org/10.1093/jxb/erv416	journal	September 2015
At the border: the plasma membrane-cell wall continuum Liu, Z.; Persson, S.; Sanchez-Rodriguez, C. Journal of Experimental Botany, Vol. 66, Issue 6 https://doi.org/10.1093/jxb/erv019	journal	February 2015
Molecular Analysis of Cellulose Biosynthesis in Arabidopsis Arioli, Tony; Peng, Liangcai; Betzner, Andreas S. Science, Vol. 279, Issue 5351 https://doi.org/10.1126/science.279.5351.717	journal	January 1998
Phylotranscriptomic analysis of the origin and early diversification of land plants Wickett, Norman J.; Mirarab, Siavash; Nguyen, Nam Proceedings of the National Academy of Sciences, Vol. 111, Issue 45 https://doi.org/10.1073/pnas.1323926111	journal	October 2014
Elucidating the Mechanisms of Assembly and Subunit Interaction of the Cellulose Synthase Complex of Arabidopsis Secondary Cell Walls Atanassov, Ivan I.; Pittman, Jon K.; Turner, Simon R. Journal of Biological Chemistry, Vol. 284, Issue 6 https://doi.org/10.1074/jbc.M807456200	journal	December 2008
Formation of wood secondary cell wall may involve two type cellulose synthase complexes in Populus Xi, Wang; Song, Dongliang; Sun, Jiayan Plant Molecular Biology, Vol. 93, Issue 4-5 https://doi.org/10.1007/s11103-016-0570-8	journal	December 2016
NorWood: a gene expression resource for evo-devo studies of conifer wood development Jokipii-Lukkari, Soile; Sundell, David; Nilsson, Ove New Phytologist, Vol. 216, Issue 2 https://doi.org/10.1111/nph.14458	journal	February 2017
Why Plants Were Terrestrial from the Beginning Harholt, Jesper; Moestrup, Øjvind; Ulvskov, Peter Trends in Plant Science, Vol. 21, Issue 2 https://doi.org/10.1016/j.tplants.2015.11.010	journal	February 2016
Cellulose Biosynthesis: Counting the Chains Jarvis, M. C. PLANT PHYSIOLOGY, Vol. 163, Issue 4 https://doi.org/10.1104/pp.113.231092	journal	December 2013
Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy Zhang, Tian; Zheng, Yunzhen; Cosgrove, Daniel J. The Plant Journal, Vol. 85, Issue 2 https://doi.org/10.1111/tpj.13102	journal	January 2016
Longevity in vivo of primary cell wall cellulose synthases Hill, Joseph Lee; Josephs, Cooper; Barnes, William J. Plant Molecular Biology, Vol. 96, Issue 3 https://doi.org/10.1007/s11103-017-0695-4	journal	January 2018
Identification of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites—a potential role in regulating protein degradation Taylor, Neil G. Plant Molecular Biology, Vol. 64, Issue 1-2 https://doi.org/10.1007/s11103-007-9142-2	journal	February 2007
Cellulose Synthesis and Its Regulation Li, Shundai; Bashline, Logan; Lei, Lei The Arabidopsis Book, Vol. 12 https://doi.org/10.1199/tab.0169	journal	January 2014
The water solubilities and heats of solution of short chain cellulosic oligosaccharides Taylor, J. B. Transactions of the Faraday Society, Vol. 53 https://doi.org/10.1039/tf9575301198	journal	January 1957
Functional Specialization of Cellulose Synthase Isoforms in a Moss Shows Parallels with Seed Plants Norris, Joanna H.; Li, Xingxing; Huang, Shixin Plant Physiology, Vol. 175, Issue 1 https://doi.org/10.1104/pp.17.00885	journal	August 2017
Plant cellulose synthesis: CESA proteins crossing kingdoms Kumar, Manoj; Turner, Simon Phytochemistry, Vol. 112 https://doi.org/10.1016/j.phytochem.2014.07.009	journal	April 2015
Catalytic Subunit Stoichiometry within the Cellulose Synthase Complex Gonneau, Martine; Desprez, Thierry; Guillot, Alain Plant Physiology, Vol. 166, Issue 4 https://doi.org/10.1104/pp.114.250159	journal	October 2014
The cellulose synthase (CESA) gene superfamily of the moss Physcomitrella patens Roberts, Alison W.; Bushoven, John T. Plant Molecular Biology, Vol. 63, Issue 2 https://doi.org/10.1007/s11103-006-9083-1	journal	September 2006
Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis Persson, S.; Paredez, A.; Carroll, A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 39 https://doi.org/10.1073/pnas.0706592104	journal	September 2007
The cellulose synthase superfamily in fully sequenced plants and algae Yin, Yanbin; Huang, Jinling; Xu, Ying BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-99	journal	January 2009
Characterization of a Functional Soluble Form of a Brassica napus Membrane-Anchored Endo-1,4-β-Glucanase Heterologously Expressed in Pichia pastoris Mølhøj, Michael; Ulvskov, Peter; Dal Degan, Florence Plant Physiology, Vol. 127, Issue 2 https://doi.org/10.1104/pp.010269	journal	October 2001
Native Cellulose: A Composite of Two Distinct Crystalline Forms Atalla, R. H.; Vanderhart, D. L. Science, Vol. 223, Issue 4633 https://doi.org/10.1126/science.223.4633.283	journal	January 1984
The Cellulase KORRIGAN Is Part of the Cellulose Synthase Complex Vain, Thomas; Crowell, Elizabeth Faris; Timpano, Hélène Plant Physiology, Vol. 165, Issue 4 https://doi.org/10.1104/pp.114.241216	journal	June 2014
Phylogenetically Distinct Cellulose Synthase Genes Support Secondary Wall Thickening in Arabidopsis Shoot Trichomes and Cotton Fiber Betancur, Lissete; Singh, Bir; Rapp, Ryan A. Journal of Integrative Plant Biology, Vol. 52, Issue 2 https://doi.org/10.1111/j.1744-7909.2010.00934.x	journal	February 2010
A single heterologously expressed plant cellulose synthase isoform is sufficient for cellulose microfibril formation in vitro Purushotham, Pallinti; Cho, Sung Hyun; Díaz-Moreno, Sara M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 40 https://doi.org/10.1073/pnas.1606210113	journal	September 2016
Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis Zhang, Tian; Mahgsoudy-Louyeh, Sahar; Tittmann, Bernhard Cellulose, Vol. 21, Issue 2 https://doi.org/10.1007/s10570-013-9996-1	journal	July 2013
Xyloglucan and its Interactions with Other Components of the Growing Cell Wall Park, Yong Bum; Cosgrove, Daniel J. Plant and Cell Physiology, Vol. 56, Issue 2 https://doi.org/10.1093/pcp/pcu204	journal	January 2015
Unique Aspects of the Structure and Dynamics of Elementary I β Cellulose Microfibrils Revealed by Computational Simulations Oehme, Daniel P.; Downton, Matthew T.; Doblin, Monika S. Plant Physiology, Vol. 168, Issue 1 https://doi.org/10.1104/pp.114.254664	journal	March 2015
Structure of native cellulose microfibrils, the starting point for nanocellulose manufacture Jarvis, Michael C. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 376, Issue 2112 https://doi.org/10.1098/rsta.2017.0045	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 Wang, Jian; Howles, Paul A.; Cork, Ann H. Plant Physiology, Vol. 142, Issue 2 https://doi.org/10.1104/pp.106.084004	journal	August 2006
Cellulose synthase complex organization and cellulose microfibril structure Turner, Simon; Kumar, Manoj Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 376, Issue 2112 https://doi.org/10.1098/rsta.2017.0048	journal	December 2017
Wide-Angle X-Ray Scattering and Solid-State Nuclear Magnetic Resonance Data Combined to Test Models for Cellulose Microfibrils in Mung Bean Cell Walls Newman, R. H.; Hill, S. J.; Harris, P. J. PLANT PHYSIOLOGY, Vol. 163, Issue 4 https://doi.org/10.1104/pp.113.228262	journal	October 2013
How Cellulose Elongates—A QM/MM Study of the Molecular Mechanism of Cellulose Polymerization in Bacterial CESA Yang, Hui; Zimmer, Jochen; Yingling, Yaroslava G. The Journal of Physical Chemistry B, Vol. 119, Issue 22 https://doi.org/10.1021/acs.jpcb.5b01433	journal	April 2015
Phosphoregulation of the Plant Cellulose Synthase Complex and Cellulose Synthase-Like Proteins Speicher, Tori; Li, Patrick; Wallace, Ian Plants, Vol. 7, Issue 3 https://doi.org/10.3390/plants7030052	journal	June 2018
Exploring Microtubule-Dependent Cellulose-Synthase-Complex Movement with High Precision Particle Tracking Woodley, Marcus; Mulvihill, Adam; Fujita, Miki Plants, Vol. 7, Issue 3 https://doi.org/10.3390/plants7030053	journal	July 2018
Turning a hobby into a job: How duplicated genes find new functions Conant, Gavin C.; Wolfe, Kenneth H. Nature Reviews Genetics, Vol. 9, Issue 12 https://doi.org/10.1038/nrg2482	journal	December 2008
Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana Desprez, T.; Juraniec, M.; Crowell, E. F. Proceedings of the National Academy of Sciences, Vol. 104, Issue 39 https://doi.org/10.1073/pnas.0706569104	journal	September 2007
BcsA and BcsB form the catalytically active core of bacterial cellulose synthase sufficient for in vitro cellulose synthesis Omadjela, O.; Narahari, A.; Strumillo, J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 44 https://doi.org/10.1073/pnas.1314063110	journal	October 2013
Two Complementary Mechanisms Underpin Cell Wall Patterning during Xylem Vessel Development Schneider, Rene; Tang, Lu; Lampugnani, Edwin R. The Plant Cell, Vol. 29, Issue 10 https://doi.org/10.1105/tpc.17.00309	journal	September 2017
Cellulose and callose synthesis and organization in focus, what's new? Schneider, René; Hanak, Tobias; Persson, Staffan Current Opinion in Plant Biology, Vol. 34 https://doi.org/10.1016/j.pbi.2016.07.007	journal	December 2016
Structure and spacing of cellulose microfibrils in woody cell walls of dicots Thomas, Lynne H.; Forsyth, V. Trevor; Martel, Anne Cellulose, Vol. 21, Issue 6 https://doi.org/10.1007/s10570-014-0431-z	journal	October 2014
Evolution of increased complexity in a molecular machine Finnigan, Gregory C.; Hanson-Smith, Victor; Stevens, Tom H. Nature, Vol. 481, Issue 7381 https://doi.org/10.1038/nature10724	journal	January 2012
Cellulose synthesis: a complex complex Mutwil, M.; Debolt, S.; Persson, S. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.007	journal	June 2008
Alleles Causing Resistance to Isoxaben and Flupoxam Highlight the Significance of Transmembrane Domains for CESA Protein Function Shim, Isaac; Law, Robert; Kileeg, Zachary Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01152	journal	August 2018
The Arabidopsis Cellulose Synthase Complex: A Proposed Hexamer of CESA Trimers in an Equimolar Stoichiometry Hill, Joseph L.; Hammudi, Mustafa B.; Tien, Ming The Plant Cell, Vol. 26, Issue 12 https://doi.org/10.1105/tpc.114.131193	journal	December 2014
Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants Li, Shundai; Bashline, Logan; Zheng, Yunzhen Proceedings of the National Academy of Sciences, Vol. 113, Issue 40 https://doi.org/10.1073/pnas.1613273113	journal	September 2016
Gaining insight into cell wall cellulose macrofibril organisation by simulating microfibril adsorption Oehme, Daniel P.; Doblin, Monika S.; Wagner, John Cellulose, Vol. 22, Issue 6 https://doi.org/10.1007/s10570-015-0778-9	journal	October 2015
The Sites of Cellulose Synthesis in Algae: Diversity and Evolution of Cellulose-Synthesizing Enzyme Complexes Tsekos, Ioannes Journal of Phycology, Vol. 35, Issue 4 https://doi.org/10.1046/j.1529-8817.1999.3540635.x	journal	August 1999
Cellulose synthases: new insights from crystallography and modeling Slabaugh, Erin; Davis, Jonathan K.; Haigler, Candace H. Trends in Plant Science, Vol. 19, Issue 2 https://doi.org/10.1016/j.tplants.2013.09.009	journal	February 2014
Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation Watanabe, Yoichiro; Schneider, Rene; Barkwill, Sarah Proceedings of the National Academy of Sciences, Vol. 115, Issue 27 https://doi.org/10.1073/pnas.1802113115	journal	June 2018
Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants Scheible, W. -R.; Eshed, R.; Richmond, T. Proceedings of the National Academy of Sciences, Vol. 98, Issue 18 https://doi.org/10.1073/pnas.191361598	journal	August 2001
A Molecular Timeline for the Origin of Photosynthetic Eukaryotes Yoon, Hwan Su; Hackett, Jeremiah D.; Ciniglia, Claudia Molecular Biology and Evolution, Vol. 21, Issue 5 https://doi.org/10.1093/molbev/msh075	journal	May 2004
Functional Analysis of Cellulose Synthase (CESA) Protein Class Specificity Kumar, Manoj; Atanassov, Ivan; Turner, Simon Plant Physiology, Vol. 173, Issue 2 https://doi.org/10.1104/pp.16.01642	journal	December 2016
Cell Wall, Cytoskeleton, and Cell Expansion in Higher Plants Bashline, Logan; Lei, Lei; Li, Shundai Molecular Plant, Vol. 7, Issue 4 https://doi.org/10.1093/mp/ssu018	journal	April 2014
A ratchet for protein complexity Doolittle, W. Ford Nature, Vol. 481, Issue 7381 https://doi.org/10.1038/nature10816	journal	January 2012
Moss cell walls: structure and biosynthesis Roberts, Alison W.; Roberts, Eric M.; Haigler, Candace H. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00166	journal	January 2012
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 Vergara, Claudia E.; Carpita, Nicholas C. Plant Molecular Biology, Vol. 47, Issue 1/2, p. 145-160 https://doi.org/10.1023/A:1010631431620	journal	September 2001
The Cell Biology of Cellulose Synthesis McFarlane, Heather E.; Döring, Anett; Persson, Staffan Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040240	journal	April 2014
Cellulose synthase ‘class specific regions’ are intrinsically disordered and functionally undifferentiated: Intrinsic disorder in cellulose synthases Scavuzzo-Duggan, Tess R.; Chaves, Arielle M.; Singh, Abhishek Journal of Integrative Plant Biology, Vol. 60, Issue 6 https://doi.org/10.1111/jipb.12637	journal	March 2018
Progress toward Understanding Protein S-acylation: Prospective in Plants Li, Yaxiao; Qi, Baoxiu Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00346	journal	March 2017
Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1A903V and CESA3T942I of cellulose synthase Harris, D. M.; Corbin, K.; Wang, T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 11 https://doi.org/10.1073/pnas.1200352109	journal	February 2012
The jiaoyao1 Mutant Is an Allele of korrigan1 That Abolishes Endoglucanase Activity and Affects the Organization of Both Cellulose Microfibrils and Microtubules in Arabidopsis Lei, Lei; Zhang, Tian; Strasser, Richard The Plant Cell, Vol. 26, Issue 6 https://doi.org/10.1105/tpc.114.126193	journal	June 2014
Cellulose Structural Polymorphism in Plant Primary Cell Walls Investigated by High-Field 2D Solid-State NMR Spectroscopy and Density Functional Theory Calculations Wang, Tuo; Yang, Hui; Kubicki, James D. Biomacromolecules, Vol. 17, Issue 6 https://doi.org/10.1021/acs.biomac.6b00441	journal	May 2016
Prediction of the structures of the plant-specific regions of vascular plant cellulose synthases and correlated functional analysis Sethaphong, Latsavongsakda; Davis, Jonathan K.; Slabaugh, Erin Cellulose, Vol. 23, Issue 1 https://doi.org/10.1007/s10570-015-0789-6	journal	October 2015
A new putative cellulose-synthesizing complex ofColeochaete scutata Okuda, K.; Brown, R. M. Protoplasma, Vol. 168, Issue 1-2 https://doi.org/10.1007/BF01332650	journal	March 1992
Interactions among three distinct CesA proteins essential for cellulose synthesis Taylor, N. G.; Howells, R. M.; Huttly, A. K. Proceedings of the National Academy of Sciences, Vol. 100, Issue 3 https://doi.org/10.1073/pnas.0337628100	journal	January 2003
A Molecular Description of Cellulose Biosynthesis McNamara, Joshua T.; Morgan, Jacob L. W.; Zimmer, Jochen Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-033930	journal	June 2015
The cell biology of secondary cell wall biosynthesis Meents, Miranda J.; Watanabe, Yoichiro; Samuels, A. Lacey Annals of Botany, Vol. 121, Issue 6 https://doi.org/10.1093/aob/mcy005	journal	February 2018
Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants Mueller, S. C. The Journal of Cell Biology, Vol. 84, Issue 2 https://doi.org/10.1083/jcb.84.2.315	journal	February 1980
Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase Chen, S.; Ehrhardt, D. W.; Somerville, C. R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 40 https://doi.org/10.1073/pnas.1012348107	journal	September 2010
Cellulose microfibril aggregates and their size variation with cell wall type Donaldson, Lloyd Wood Science and Technology, Vol. 41, Issue 5 https://doi.org/10.1007/s00226-006-0121-6	journal	January 2007
Cellulose synthesis in the Arabidopsis secondary cell wall Taylor, Neil G.; Gardiner, John C.; Whiteman, Raymond Cellulose, Vol. 11, Issue 3/4 https://doi.org/10.1023/B:CELL.0000046405.11326.a8	journal	September 2004
Imaging cellulose synthase motility during primary cell wall synthesis in the grass Brachypodium distachyon Liu, Derui; Zehfroosh, Nina; Hancock, Brandon L. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-14988-4	journal	November 2017
The Structure of the Catalytic Domain of a Plant Cellulose Synthase and Its Assembly into Dimers Olek, Anna T.; Rayon, Catherine; Makowski, Lee The Plant Cell, Vol. 26, Issue 7 https://doi.org/10.1105/tpc.114.126862	journal	July 2014
A Structural Study of CESA1 Catalytic Domain of Arabidopsis Cellulose Synthesis Complex: Evidence for CESA Trimers Vandavasi, Venu Gopal; Putnam, Daniel K.; Zhang, Qiu Plant Physiology, Vol. 170, Issue 1 https://doi.org/10.1104/pp.15.01356	journal	November 2015
Plasmodesmata: a freeze-fracture view Willison, J. H. M. Canadian Journal of Botany, Vol. 54, Issue 24 https://doi.org/10.1139/b76-304	journal	December 1976
Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Wong, H. C.; Fear, A. L.; Calhoon, R. D. Proceedings of the National Academy of Sciences, Vol. 87, Issue 20 https://doi.org/10.1073/pnas.87.20.8130	journal	October 1990
Structure characterization of native cellulose during dehydration and rehydration Fang, Lin; Catchmark, Jeffrey M. Cellulose, Vol. 21, Issue 6 https://doi.org/10.1007/s10570-014-0435-8	journal	September 2014
Understanding Plant Cellulose Synthases through a Comprehensive Investigation of the Cellulose Synthase Family Sequences Carroll, Andrew; Specht, Chelsea D. Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00005	journal	January 2011
An update on the nomenclature for the cellulose synthase genes in Populus Kumar, Manoj; Thammannagowda, Shivegowda; Bulone, Vincent Trends in Plant Science, Vol. 14, Issue 5 https://doi.org/10.1016/j.tplants.2009.02.004	journal	May 2009
Domain swaps of Arabidopsis secondary wall cellulose synthases to elucidate their class specificity Hill, Joseph Lee; Hill, Ashley Nicole; Roberts, Alison W. Plant Direct, Vol. 2, Issue 7 https://doi.org/10.1002/pld3.61	journal	July 2018
Interaction between Cellooligosaccharides in Aqueous Solution from Molecular Dynamics Simulation: Comparison of Cellotetraose, Cellopentaose, and Cellohexaose Umemura, Myco; Yuguchi, Yoshiaki; Hirotsu, Takahiro The Journal of Physical Chemistry A, Vol. 108, Issue 34 https://doi.org/10.1021/jp049044a	journal	August 2004
Tertiary model of a plant cellulose synthase Sethaphong, L.; Haigler, C. H.; Kubicki, J. D. Proceedings of the National Academy of Sciences, Vol. 110, Issue 18 https://doi.org/10.1073/pnas.1301027110	journal	April 2013
Rice Cellulose SynthaseA8 Plant-Conserved Region Is a Coiled-Coil at the Catalytic Core Entrance Rushton, Phillip S.; Olek, Anna T.; Makowski, Lee Plant Physiology, Vol. 173, Issue 1 https://doi.org/10.1104/pp.16.00739	journal	November 2016
Characterization of cellulose synthase complexes in Populus xylem differentiation Song, Dongliang; Shen, Junhui; Li, Laigeng New Phytologist, Vol. 187, Issue 3 https://doi.org/10.1111/j.1469-8137.2010.03315.x	journal	June 2010
Nanostructure of cellulose microfibrils in spruce wood Fernandes, A. N.; Thomas, L. H.; Altaner, C. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 47 https://doi.org/10.1073/pnas.1108942108	journal	November 2011
Exploiting CELLULOSE SYNTHASE (CESA) Class Specificity to Probe Cellulose Microfibril Biosynthesis Kumar, Manoj; Mishra, Laxmi; Carr, Paul Plant Physiology, Vol. 177, Issue 1 https://doi.org/10.1104/pp.18.00263	journal	March 2018
Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Pear, J. R.; Kawagoe, Y.; Schreckengost, W. E. Proceedings of the National Academy of Sciences, Vol. 93, Issue 22 https://doi.org/10.1073/pnas.93.22.12637	journal	October 1996
Analysis of cell-wall polymers during cotton fiber development Timpa, JudyD.; Triplett, BarbaraA. Planta, Vol. 189, Issue 1 https://doi.org/10.1007/BF00201350	journal	January 1993
CELLULOSE BIOSYNTHESIS: Exciting Times for A Difficult Field of Study Delmer, Deborah P. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.arplant.50.1.245	journal	June 1999
Probing the Molecular Architecture of Arabidopsis thaliana Secondary Cell Walls Using Two- and Three-Dimensional ¹³ C Solid State Nuclear Magnetic Resonance Spectroscopy Dupree, Ray; Simmons, Thomas J.; Mortimer, Jennifer C. Biochemistry, Vol. 54, Issue 14 https://doi.org/10.1021/bi501552k	journal	March 2015
Molecular Modeling and Imaging of Initial Stages of Cellulose Fibril Assembly: Evidence for a Disordered Intermediate Stage Haigler, Candace H.; Grimson, Mark J.; Gervais, Julien PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0093981	journal	April 2014
Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls Giddings, T. H. The Journal of Cell Biology, Vol. 84, Issue 2 https://doi.org/10.1083/jcb.84.2.327	journal	February 1980
Ultrastructure and Formation of Plant Cell Walls Muhlethaler, K. Annual Review of Plant Physiology, Vol. 18, Issue 1 https://doi.org/10.1146/annurev.pp.18.060167.000245	journal	June 1967
The Shape of Native Plant Cellulose Microfibrils Kubicki, James D.; Yang, Hui; Sawada, Daisuke Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-32211-w	journal	September 2018
Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis Primary Cell Walls: Evidence from Solid-State Nuclear Magnetic Resonance Wang, Tuo; Park, Yong Bum; Cosgrove, Daniel J. Plant Physiology, Vol. 168, Issue 3 https://doi.org/10.1104/pp.15.00665	journal	June 2015
A survey of plant and algal genomes and transcriptomes reveals new insights into the evolution and function of the cellulose synthase superfamily Yin, Yanbin; Johns, Mitrick A.; Cao, Huansheng BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-260	journal	January 2014
Synthesis and Self-Assembly of Cellulose Microfibrils from Reconstituted Cellulose Synthase Cho, Sung Hyun; Purushotham, Pallinti; Fang, Chao Plant Physiology, Vol. 175, Issue 1 https://doi.org/10.1104/pp.17.00619	journal	August 2017
Distribution of plasma membrane rosettes and kinetics of cellulose formation in xylem development of higher plants Schneider, B.; Herth, W. Protoplasma, Vol. 131, Issue 2 https://doi.org/10.1007/BF01285036	journal	June 1986
PtrCel9A6, an Endo-1,4-β-Glucanase, Is Required for Cell Wall Formation during Xylem Differentiation in Populus Yu, Liangliang; Sun, Jiayan; Li, Laigeng Molecular Plant, Vol. 6, Issue 6 https://doi.org/10.1093/mp/sst104	journal	November 2013
Chemical, ultrastructural and supramolecular analysis of tension wood in Populus tremula x alba as a model substrate for reduced recalcitrance Foston, Marcus; Hubbell, Christopher A.; Samuel, Reichel Energy & Environmental Science, Vol. 4, Issue 12 https://doi.org/10.1039/c1ee02073k	journal	January 2011
Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules Paredez, A. R. Science, Vol. 312, Issue 5779 https://doi.org/10.1126/science.1126551	journal	June 2006
Cellulose Synthesis and Cell Expansion Are Regulated by Different Mechanisms in Growing Arabidopsis Hypocotyls Ivakov, Alexander; Flis, Anna; Apelt, Federico The Plant Cell, Vol. 29, Issue 6 https://doi.org/10.1105/tpc.16.00782	journal	May 2017
Cellulose Synthases and Synthesis in Arabidopsis Endler, Anne; Persson, Staffan Molecular Plant, Vol. 4, Issue 2 https://doi.org/10.1093/mp/ssq079	journal	March 2011
Cellulose Synthase Stoichiometry in Aspen Differs from Arabidopsis and Norway Spruce Zhang, Xueyang; Dominguez, Pia Guadalupe; Kumar, Manoj Plant Physiology, Vol. 177, Issue 3 https://doi.org/10.1104/pp.18.00394	journal	May 2018
Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics Brown, David M.; Zeef, Leo A. H.; Ellis, Joanne The Plant Cell, Vol. 17, Issue 8 https://doi.org/10.1105/tpc.105.031542	journal	June 2005
Immunogold Labeling of Rosette Terminal Cellulose-Synthesizing Complexes in the Vascular Plant Vigna angularis Kimura, Satoshi; Laosinchai, Walairat; Itoh, Takao The Plant Cell, Vol. 11, Issue 11 https://doi.org/10.1105/tpc.11.11.2075	journal	November 1999
Collapsed Xylem Phenotype of Arabidopsis Identifies Mutants Deficient in Cellulose Deposition in the Secondary Cell Wall Turner, S. R.; Somerville, C. R. The Plant Cell, Vol. 9, Issue 5, p. 689-701 https://doi.org/10.1105/tpc.9.5.689	journal	May 1997
Global expression analysis of CESA and CSL genes in Arabidopsis Hamann, Thorsten; Osborne, Erin; Youngs, Heather L. Cellulose, Vol. 11, Issue 3/4 https://doi.org/10.1023/B:CELL.0000046340.99925.57	journal	September 2004
Genetic modification in cellulose-synthase reduces crystallinity and improves biochemical conversion to fermentable sugar Harris, Darby; Stork, Jozsef; Debolt, Seth GCB Bioenergy, Vol. 1, Issue 1 https://doi.org/10.1111/j.1757-1707.2009.01000.x	journal	February 2009
Comprehensive analysis of cellulose content, crystallinity, and lateral packing in Gossypium hirsutum and Gossypium barbadense cotton fibers using sum frequency generation, infrared and Raman spectroscopy, and X-ray diffraction Lee, Christopher M.; Kafle, Kabindra; Belias, David W. Cellulose, Vol. 22, Issue 2 https://doi.org/10.1007/s10570-014-0535-5	journal	January 2015
Visualization of cellulose synthases in Arabidopsis secondary cell walls Watanabe, Y.; Meents, M. J.; McDonnell, L. M. Science, Vol. 350, Issue 6257 https://doi.org/10.1126/science.aac7446	journal	October 2015
The timescale of early land plant evolution Morris, Jennifer L.; Puttick, Mark N.; Clark, James W. Proceedings of the National Academy of Sciences, Vol. 115, Issue 10 https://doi.org/10.1073/pnas.1719588115	journal	February 2018
Update on Mechanisms of Plant Cell Wall Biosynthesis: How Plants Make Cellulose and Other (1→4)-β-d-Glycans Carpita, Nicholas C. Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.163360	journal	November 2010
The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution Lang, Daniel; Ullrich, Kristian K.; Murat, Florent The Plant Journal, Vol. 93, Issue 3 https://doi.org/10.1111/tpj.13801	journal	January 2018
Unidirectional Movement of Cellulose Synthase Complexes in Arabidopsis Seed Coat Epidermal Cells Deposit Cellulose Involved in Mucilage Extrusion, Adherence, and Ray Formation Griffiths, Jonathan S.; Šola, Krešimir; Kushwaha, Rekha Plant Physiology, Vol. 168, Issue 2 https://doi.org/10.1104/pp.15.00478	journal	April 2015
Manipulating cellulose biosynthesis by expression of mutant Arabidopsis proM24::CESA3 ^ixr1-2 gene in transgenic tobacco Sahoo, Dipak K.; Stork, Jozsef; DeBolt, Seth Plant Biotechnology Journal, Vol. 11, Issue 3 https://doi.org/10.1111/pbi.12024	journal	December 2012
The cytoplasmic domain of the cellulose-synthesizing complex in vascular plants Bowling, A. J.; Brown, R. M. Protoplasma, Vol. 233, Issue 1-2 https://doi.org/10.1007/s00709-008-0302-2	journal	August 2008
Large-Scale Co-Expression Approach to Dissect Secondary Cell Wall Formation Across Plant Species Ruprecht, Colin; Mutwil, Marek; Saxe, Friederike Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00023	journal	January 2011
Cellulose Biosynthesis Delmer, D. P. Annual Review of Plant Physiology, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.pp.38.060187.001355	journal	June 1987
The anisotropy1 D604N Mutation in the Arabidopsis Cellulose Synthase1 Catalytic Domain Reduces Cell Wall Crystallinity and the Velocity of Cellulose Synthase Complexes Fujita, Miki; Himmelspach, Regina; Ward, Juliet Plant Physiology, Vol. 162, Issue 1 https://doi.org/10.1104/pp.112.211565	journal	March 2013
Structure of cellulose microfibrils in mature cotton fibres Martínez-Sanz, Marta; Pettolino, Filomena; Flanagan, Bernadine Carbohydrate Polymers, Vol. 175 https://doi.org/10.1016/j.carbpol.2017.07.090	journal	November 2017
The Emerging Role of Protein Phosphorylation as a Critical Regulatory Mechanism Controlling Cellulose Biosynthesis Jones, Danielle M.; Murray, Christian M.; Ketelaar, KassaDee J. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00684	journal	May 2016
Re-constructing our models of cellulose and primary cell wall assembly Cosgrove, Daniel J. Current Opinion in Plant Biology, Vol. 22 https://doi.org/10.1016/j.pbi.2014.11.001	journal	December 2014
The Cellulose Synthase Complex: A Polymerization Driven Supramolecular Motor Diotallevi, Fabiana; Mulder, Bela Biophysical Journal, Vol. 92, Issue 8 https://doi.org/10.1529/biophysj.106.099473	journal	April 2007
What Do We Really Know about Cellulose Biosynthesis in Higher Plants? Guerriero, Gea; Fugelstad, Johanna; Bulone, Vincent Journal of Integrative Plant Biology, Vol. 52, Issue 2 https://doi.org/10.1111/j.1744-7909.2010.00935.x	journal	February 2010
Widespread Whole Genome Duplications Contribute to Genome Complexity and Species Diversity in Angiosperms Ren, Ren; Wang, Haifeng; Guo, Chunce Molecular Plant, Vol. 11, Issue 3 https://doi.org/10.1016/j.molp.2018.01.002	journal	March 2018

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A density functional theory study on the shape of the primary cellulose microfibril in plants: effects of C6 exocyclic group conformation and H-bonding Yang, Hui; Kubicki, James D. Cellulose, Vol. 27, Issue 5 https://doi.org/10.1007/s10570-020-02970-9	journal	January 2020
Convergent evolution of hetero‐oligomeric cellulose synthesis complexes in mosses and seed plants Li, Xingxing; Speicher, Tori L.; Dees, Dianka C. T. The Plant Journal https://doi.org/10.1111/tpj.14366	journal	May 2019

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