Super-resolution imaging illuminates new dynamic behaviors of cellulose synthase

Duncombe, Sydney G.; Chethan, Samir G.; Anderson, Charles T.

doi:10.1093/plcell/koab227

Title: Super-resolution imaging illuminates new dynamic behaviors of cellulose synthase

Journal Article · 14 September 2021 · The Plant Cell

DOI: https://doi.org/10.1093/plcell/koab227 · OSTI ID:1841298

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Abstract Confocal imaging has shown that CELLULOSE SYNTHASE (CESA) particles move through the plasma membrane as they synthesize cellulose. However, the resolution limit of confocal microscopy circumscribes what can be discovered about these tiny biosynthetic machines. Here, we applied Structured Illumination Microscopy (SIM), which improves resolution two-fold over confocal or widefield imaging, to explore the dynamic behaviors of CESA particles in living plant cells. SIM imaging reveals that Arabidopsis thaliana CESA particles are more than twice as dense in the plasma membrane as previously estimated, helping explain the dense arrangement of cellulose observed in new wall layers. CESA particles tracked by SIM display minimal variation in velocity, suggesting coordinated control of CESA catalytic activity within single complexes and that CESA complexes might move steadily in tandem to generate larger cellulose fibrils or bundles. SIM data also reveal that CESA particles vary in their overlaps with microtubule tracks and can complete U-turns without changing speed. CESA track patterns can vary widely between neighboring cells of similar shape, implying that cellulose patterning is not the sole determinant of cellular growth anisotropy. Together, these findings highlight SIM as a powerful tool to advance CESA imaging beyond the resolution limit of conventional light microscopy.

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Research Organization:: Northwestern Univ., Evanston, IL (United States); Pennsylvania State Univ., University Park, PA (United States). Center for Lignocellulose Structure and Formation

Sponsoring Organization:: National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0001090; SC0021314

OSTI ID:: 1841298

Journal Information:: The Plant Cell, Journal Name: The Plant Cell Journal Issue: 1 Vol. 34; ISSN 1040-4651

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (46)

Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L. Herth, Werner Planta, Vol. 164, Issue 1 https://doi.org/10.1007/BF00391020	journal	January 1985
The plasma membrane of the Funaria caulonema tip cell: morphology and distribution of particle rosettes, and the kinetics of cellulose synthesis Reiss, Hans-Dieter; Schnepf, Eberhard; Herth, Werner Planta, Vol. 160, Issue 5 https://doi.org/10.1007/BF00429759	journal	April 1984
A historical perspective on the regulation of cellulose biosynthesis Allen, Holly; Wei, Donghui; Gu, Ying Carbohydrate Polymers, Vol. 252 https://doi.org/10.1016/j.carbpol.2020.117022	journal	January 2021
A Receptor-like Kinase Mediates the Response of Arabidopsis Cells to the Inhibition of Cellulose Synthesis Hématy, Kian; Sado, Pierre-Etienne; Van Tuinen, Ageeth Current Biology, Vol. 17, Issue 11 https://doi.org/10.1016/j.cub.2007.05.018	journal	June 2007
The Control of Growth Symmetry Breaking in the Arabidopsis Hypocotyl Peaucelle, Alexis; Wightman, Raymond; Höfte, Herman Current Biology, Vol. 25, Issue 13 https://doi.org/10.1016/j.cub.2015.05.022	journal	June 2015
Interaction between Autonomous and Microtubule Guidance Systems Controls Cellulose Synthase Trajectories Chan, Jordi; Coen, Enrico Current Biology, Vol. 30, Issue 5 https://doi.org/10.1016/j.cub.2019.12.066	journal	March 2020
Microtubules and cellulose biosynthesis: the emergence of new players Li, Shundai; Lei, Lei; Yingling, Yaroslava G. Current Opinion in Plant Biology, Vol. 28 https://doi.org/10.1016/j.pbi.2015.09.002	journal	December 2015
Finding order in a bustling construction zone: quantitative imaging and analysis of cell wall assembly in plants Anderson, Charles T. Current Opinion in Plant Biology, Vol. 46 https://doi.org/10.1016/j.pbi.2018.07.014	journal	December 2018
High-Resolution Field Emission Scanning Electron Microscopy (FESEM) Imaging of Cellulose Microfibril Organization in Plant Primary Cell Walls Zheng, Yunzhen; Cosgrove, Daniel J.; Ning, Gang Microscopy and Microanalysis, Vol. 23, Issue 5 https://doi.org/10.1017/S143192761701251X	journal	August 2017
Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments Gutierrez, Ryan; Lindeboom, Jelmer J.; Paredez, Alex R. Nature Cell Biology, Vol. 11, Issue 7 https://doi.org/10.1038/ncb1886	journal	June 2009
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images Boudaoud, Arezki; Burian, Agata; Borowska-Wykręt, Dorota Nature Protocols, Vol. 9, Issue 2 https://doi.org/10.1038/nprot.2014.024	journal	January 2014
Superresolution live imaging of plant cells using structured illumination microscopy Komis, George; Mistrik, Martin; Šamajová, Olga Nature Protocols, Vol. 10, Issue 8 https://doi.org/10.1038/nprot.2015.083	journal	July 2015
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
Comparative Structural and Computational Analysis Supports Eighteen Cellulose Synthases in the Plant Cellulose Synthesis Complex Nixon, B. Tracy; Mansouri, Katayoun; Singh, Abhishek Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep28696	journal	June 2016
Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. SHORT COMMUNICATION Gustafsson, M. G. L. Journal of Microscopy, Vol. 198, Issue 2 https://doi.org/10.1046/j.1365-2818.2000.00710.x	journal	May 2000
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
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
Identification of a cellulose synthase-associated protein required for cellulose biosynthesis Gu, Y.; Kaplinsky, N.; Bringmann, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 29 https://doi.org/10.1073/pnas.1007092107	journal	July 2010
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 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
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
BRASSINOSTEROID INSENSITIVE2 negatively regulates cellulose synthesis in Arabidopsis by phosphorylating cellulose synthase 1 Sánchez-Rodríguez, Clara; Ketelaar, KassaDee; Schneider, Rene Proceedings of the National Academy of Sciences, Vol. 114, Issue 13 https://doi.org/10.1073/pnas.1615005114	journal	March 2017
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
Structure of Arabidopsis CESA3 catalytic domain with its substrate UDP-glucose provides insight into the mechanism of cellulose synthesis Qiao, Zhu; Lampugnani, Edwin R.; Yan, Xin-Fu Proceedings of the National Academy of Sciences, Vol. 118, Issue 11 https://doi.org/10.1073/pnas.2024015118	journal	March 2021
Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency Cutler, S. R.; Ehrhardt, D. W.; Griffitts, J. S. Proceedings of the National Academy of Sciences, Vol. 97, Issue 7 https://doi.org/10.1073/pnas.97.7.3718	journal	March 2000
Molecular counting by photobleaching in protein complexes with many subunits: best practices and application to the cellulose synthesis complex Chen, Yalei; Deffenbaugh, Nathan C.; Anderson, Charles T. Molecular Biology of the Cell, Vol. 25, Issue 22 https://doi.org/10.1091/mbc.e14-06-1146	journal	November 2014
Structured illumination approaches for super-resolution in plant cells Shaw, Sidney L.; Thoms, David; Powers, James Microscopy, Vol. 68, Issue 1 https://doi.org/10.1093/jmicro/dfy043	journal	October 2018
Super-Resolution Imaging of Plasmodesmata Using Three-Dimensional Structured Illumination Microscopy Fitzgibbon, Jessica; Bell, Karen; King, Emma Plant Physiology, Vol. 153, Issue 4 https://doi.org/10.1104/pp.110.157941	journal	May 2010
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
The Endocytosis of Cellulose Synthase in Arabidopsis Is Dependent on μ2, a Clathrin-Mediated Endocytosis Adaptin Bashline, Logan; Li, Shundai; Anderson, Charles T. Plant Physiology, Vol. 163, Issue 1 https://doi.org/10.1104/pp.113.221234	journal	July 2013
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
Xyloglucan Deficiency Disrupts Microtubule Stability and Cellulose Biosynthesis in Arabidopsis, Altering Cell Growth and Morphogenesis Xiao, Chaowen; Zhang, Tian; Zheng, Yunzhen Plant Physiology, Vol. 170, Issue 1 https://doi.org/10.1104/pp.15.01395	journal	November 2015
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
Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis Du, Juan; Kirui, Alex; Huang, Shixin The Plant Cell, Vol. 32, Issue 11 https://doi.org/10.1105/tpc.20.00252	journal	September 2020
A pyramid approach to subpixel registration based on intensity Thevenaz, P.; Ruttimann, U. E.; Unser, M. IEEE Transactions on Image Processing, Vol. 7, Issue 1 https://doi.org/10.1109/83.650848	journal	January 1998
Structural insights into homotrimeric assembly of cellulose synthase CesA7 from Gossypium hirsutum Zhang, Xiangnan; Xue, Yuan; Guan, Zeyuan Plant Biotechnology Journal, Vol. 19, Issue 8 https://doi.org/10.1111/pbi.13571	journal	April 2021
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
Cytosolic invertases contribute to cellulose biosynthesis and influence carbon partitioning in seedlings of Arabidopsis thaliana Barnes, William J.; Anderson, Charles T. The Plant Journal, Vol. 94, Issue 6 https://doi.org/10.1111/tpj.13909	journal	April 2018
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
Architecture of a catalytically active homotrimeric plant cellulose synthase complex Purushotham, Pallinti; Ho, Ruoya; Zimmer, Jochen Science, Vol. 369, Issue 6507 https://doi.org/10.1126/science.abb2978	journal	July 2020
Dynamic Construction, Perception, and Remodeling of Plant Cell Walls Anderson, Charles T.; Kieber, Joseph J. Annual Review of Plant Biology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-arplant-081519-035846	journal	April 2020
Anisotropic Expansion of the Plant cell wall Baskin, Tobias I. Annual Review of Cell and Developmental Biology, Vol. 21, Issue 1 https://doi.org/10.1146/annurev.cellbio.20.082503.103053	journal	November 2005
The rotation of cellulose synthase trajectories is microtubule dependent and influences the texture of epidermal cell walls in Arabidopsis hypocotyls Chan, J.; Crowell, E.; Eder, M. Journal of Cell Science, Vol. 123, Issue 20 https://doi.org/10.1242/jcs.074641	journal	September 2010
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
KymoButler, a deep learning software for automated kymograph analysis Jakobs, Maximilian AH; Dimitracopoulos, Andrea; Franze, Kristian eLife, Vol. 8 https://doi.org/10.7554/eLife.42288	journal	August 2019

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59 BASIC BIOLOGICAL SCIENCES
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Title: Super-resolution imaging illuminates new dynamic behaviors of cellulose synthase

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