Tissue-specific directionality of cellulose synthase complex movement inferred from cellulose microfibril polarity in secondary cell walls of Arabidopsis

Choi, Juseok; Makarem, Mohamadamin; Lee, Chonghan; Lee, Jongcheol; Kiemle, Sarah; Cosgrove, Daniel J.; Kim, Seong H.

doi:10.1038/s41598-023-48545-z

Tissue-specific directionality of cellulose synthase complex movement inferred from cellulose microfibril polarity in secondary cell walls of Arabidopsis

Journal Article · Tue Dec 12 00:00:00 EST 2023 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-023-48545-z· OSTI ID:2352285

Choi, Juseok ^[1]; Makarem, Mohamadamin ^[2]; Lee, Chonghan ^[2]; Lee, Jongcheol ^[2]; Kiemle, Sarah ^[2]; ^[2]; ^[2]

Pennsylvania State University, University Park, PA (United States); Pennsylvania State University
Pennsylvania State University, University Park, PA (United States)

In plant cells, cellulose synthase complexes (CSCs) are nanoscale machines that synthesize and extrude crystalline cellulose microfibrils (CMFs) into the apoplast where CMFs are assembled with other matrix polymers into specific structures. We report the tissue-specific directionality of CSC movements of the xylem and interfascicular fiber walls of Arabidopsis stems, inferred from the polarity of CMFs determined using vibrational sum frequency generation spectroscopy. CMFs in xylems are deposited in an unidirectionally biased pattern with their alignment axes tilted about 25° off the stem axis, while interfascicular fibers are bidirectional and highly aligned along the longitudinal axis of the stem. These structures are compatible with the design of fiber-reinforced composites for tubular conduit and support pillar, respectively, suggesting that during cell development, CSC movement is regulated to produce wall structures optimized for cell-specific functions.

View Accepted Manuscript (DOE)

Research Organization:: Pennsylvania State University, University Park, PA (United States)

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

Grant/Contract Number:: SC0001090

OSTI ID:: 2352285

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 13; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (53)

Phenotypic effects of changes in the FTVTxK region of an Arabidopsis secondary wall cellulose synthase compared with results from analogous mutations in other isoforms Burris, Jason N.; Makarem, Mohamadamin; Slabaugh, Erin Plant Direct, Vol. 5, Issue 8 https://doi.org/10.1002/pld3.335	journal	August 2021
About the structure of cellulose: debating the Lindman hypothesis Glasser, Wolfgang G.; Atalla, Rajai H.; Blackwell, John Cellulose, Vol. 19, Issue 3 https://doi.org/10.1007/s10570-012-9691-7	journal	March 2012
Vibrational sum-frequency-generation (SFG) spectroscopy study of the structural assembly of cellulose microfibrils in reaction woods Kafle, Kabindra; Shi, Rui; Lee, Christopher M. Cellulose, Vol. 21, Issue 4 https://doi.org/10.1007/s10570-014-0322-3	journal	June 2014
Isolation and handedness of helical coiled cellulosic thickenings from plant petiole tracheary elements Gray, Derek G. Cellulose, Vol. 21, Issue 5 https://doi.org/10.1007/s10570-014-0382-4	journal	August 2014
Probing cellulose structures with vibrational spectroscopy Makarem, Mohamadamin; Lee, Christopher M.; Kafle, Kabindra Cellulose, Vol. 26, Issue 1 https://doi.org/10.1007/s10570-018-2199-z	journal	January 2019
Moisture-related changes in the nanostructure of woods studied with X-ray and neutron scattering Penttilä, Paavo A.; Altgen, Michael; Carl, Nico Cellulose, Vol. 27, Issue 1 https://doi.org/10.1007/s10570-019-02781-7	journal	October 2019
Correlation between crystalline cellulose structure and cellulose synthase complex shape: a spectroscopic study with unicellular freshwater alga Micrasterias Huang, Shixin; Kiemle, Sarah N.; Makarem, Mohamadamin Cellulose, Vol. 27, Issue 1 https://doi.org/10.1007/s10570-019-02793-3	journal	October 2019
Magnetic field effects on cellulose nanocrystal ordering in a non-aqueous solvent Barhoumi Meddeb, Amira; Chae, Inseok; Han, Aijie Cellulose, Vol. 27, Issue 14 https://doi.org/10.1007/s10570-020-03320-5	journal	July 2020
Design of fiber-reinforced composite pressure vessels under various loading conditions Parnas, Levend; Katırcı, Nuran Composite Structures, Vol. 58, Issue 1 https://doi.org/10.1016/S0263-8223(02)00037-5	journal	October 2002
Dehydration-induced physical strains of cellulose microfibrils in plant cell walls Huang, Shixin; Makarem, Mohamadamin; Kiemle, Sarah N. Carbohydrate Polymers, Vol. 197 https://doi.org/10.1016/j.carbpol.2018.05.091	journal	October 2018
Shear-induced unidirectional deposition of bacterial cellulose microfibrils using rising bubble stream cultivation Chae, Inseok; Bokhari, Syed M. Q.; Chen, Xing Carbohydrate Polymers, Vol. 255 https://doi.org/10.1016/j.carbpol.2020.117328	journal	March 2021
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
Cellulose microfibril angle in the cell wall of wood fibres Barnett, J. R.; Bonham, Victoria A. Biological Reviews, Vol. 79, Issue 2 https://doi.org/10.1017/S1464793103006377	journal	January 1999
Distinguishing Mesoscale Polar Order (Unidirectional vs Bidirectional) of Cellulose Microfibrils in Plant Cell Walls Using Sum Frequency Generation Spectroscopy Makarem, Mohamadamin; Nishiyama, Yoshiharu; Xin, Xiaoran The Journal of Physical Chemistry B, Vol. 124, Issue 37 https://doi.org/10.1021/acs.jpcb.0c07076	journal	August 2020
Numerical Simulation of Vibrational Sum Frequency Generation Intensity for Non-Centrosymmetric Domains Interspersed in an Amorphous Matrix: A Case Study for Cellulose in Plant Cell Wall Choi, Juseok; Lee, Jongcheol; Makarem, Mohamadamin The Journal of Physical Chemistry B, Vol. 126, Issue 35 https://doi.org/10.1021/acs.jpcb.2c03897	journal	August 2022
Multimodal Broadband Vibrational Sum Frequency Generation (MM-BB-V-SFG) Spectrometer and Microscope Lee, Christopher M.; Kafle, Kabindra; Huang, Shixin The Journal of Physical Chemistry B, Vol. 120, Issue 1 https://doi.org/10.1021/acs.jpcb.5b10290	journal	December 2015
Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy Huang, Shixin; Makarem, Mohamadamin; Kiemle, Sarah N. The Journal of Physical Chemistry B, Vol. 122, Issue 19 https://doi.org/10.1021/acs.jpcb.8b01537	journal	April 2018
Dependence of Sum Frequency Generation (SFG) Spectral Features on the Mesoscale Arrangement of SFG-Active Crystalline Domains Interspersed in SFG-Inactive Matrix: A Case Study with Cellulose in Uniaxially Aligned Control Samples and Alkali-Treated Secondary Cell Walls of Plants Makarem, Mohamadamin; Sawada, Daisuke; O’Neill, Hugh M. The Journal of Physical Chemistry C, Vol. 121, Issue 18 https://doi.org/10.1021/acs.jpcc.7b02770	journal	May 2017
Experimental and Theoretical Study of Azimuth Angle and Polarization Dependences of Sum-Frequency-Generation Vibrational Spectral Features of Uniaxially Aligned Cellulose Crystals Chen, Xing; Lee, Christopher M.; Wang, Hong-Fei The Journal of Physical Chemistry C, Vol. 121, Issue 34 https://doi.org/10.1021/acs.jpcc.7b03037	journal	August 2017
Selective Detection of Crystalline Cellulose in Plant Cell Walls with Sum-Frequency-Generation (SFG) Vibration Spectroscopy Barnette, Anna L.; Bradley, Laura C.; Veres, Brandon D. Biomacromolecules, Vol. 12, Issue 7 https://doi.org/10.1021/bm200518n	journal	July 2011
Effects of Plant Cell Wall Matrix Polysaccharides on Bacterial Cellulose Structure Studied with Vibrational Sum Frequency Generation Spectroscopy and X-ray Diffraction Park, Yong Bum; Lee, Christopher M.; Kafle, Kabindra Biomacromolecules, Vol. 15, Issue 7 https://doi.org/10.1021/bm500567v	journal	May 2014
Crystal Structure and Hydrogen-Bonding System in Cellulose Iβ from Synchrotron X-ray and Neutron Fiber Diffraction Nishiyama, Yoshiharu; Langan, Paul; Chanzy, Henri Journal of the American Chemical Society, Vol. 124, Issue 31 https://doi.org/10.1021/ja0257319	journal	August 2002
Cellulose Microfibril Twist, Mechanics, and Implication for Cellulose Biosynthesis Zhao, Zhen; Shklyaev, Oleg E.; Nili, Abdolmajid The Journal of Physical Chemistry A, Vol. 117, Issue 12 https://doi.org/10.1021/jp3089929	journal	March 2013
The perceptron: A probabilistic model for information storage and organization in the brain. Rosenblatt, F. Psychological Review, Vol. 65, Issue 6 https://doi.org/10.1037/h0042519	journal	January 1958
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
Growth of the plant cell wall Cosgrove, Daniel J. Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861 https://doi.org/10.1038/nrm1746	journal	November 2005
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
Electron microdiffraction reveals the nanoscale twist geometry of cellulose nanocrystals Ogawa, Yu Nanoscale, Vol. 11, Issue 45 https://doi.org/10.1039/C9NR06044H	journal	January 2019
Probing crystal structure and mesoscale assembly of cellulose microfibrils in plant cell walls, tunicate tests, and bacterial films using vibrational Sum Frequency Generation (SFG) spectroscopy Lee, Christopher M.; Kafle, Kabindra; Park, Yong Bum Physical Chemistry Chemical Physics, Vol. 16, Issue 22 https://doi.org/10.1039/c4cp00515e	journal	January 2014
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
Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes Li, S.; Lei, L.; Somerville, C. R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 1 https://doi.org/10.1073/pnas.1118560109	journal	December 2011
New twist on artificial muscles Haines, Carter S.; Li, Na; Spinks, Geoffrey M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 42 https://doi.org/10.1073/pnas.1605273113	journal	September 2016
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
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
Cellulose nanocrystals: a versatile nanoplatform for emerging biomedical applications Sunasee, Rajesh; Hemraz, Usha D.; Ckless, Karina Expert Opinion on Drug Delivery, Vol. 13, Issue 9 https://doi.org/10.1080/17425247.2016.1182491	journal	May 2016
Secondary Cell Walls: Biosynthesis, Patterned Deposition and Transcriptional Regulation Zhong, Ruiqin; Ye, Zheng-Hua Plant and Cell Physiology, Vol. 56, Issue 2 https://doi.org/10.1093/pcp/pcu140	journal	October 2014
Monitoring Meso-Scale Ordering of Cellulose in Intact Plant Cell Walls Using Sum Frequency Generation Spectroscopy Park, Y. B.; Lee, C. M.; Koo, B. -W. PLANT PHYSIOLOGY, Vol. 163, Issue 2 https://doi.org/10.1104/pp.113.225235	journal	August 2013
Fibers. A Model for Studying Cell Differentiation, Cell Elongation, and Cell Wall Biosynthesis Zhong, Ruiqin; Burk, David H.; Ye, Zheng-Hua Plant Physiology, Vol. 126, Issue 2 https://doi.org/10.1104/pp.126.2.477	journal	June 2001
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
Alteration of Oriented Deposition of Cellulose Microfibrils by Mutation of a Katanin-Like Microtubule-Severing Protein Burk, David H.; Ye, Zheng-Hua The Plant Cell, Vol. 14, Issue 9 https://doi.org/10.1105/tpc.003947	journal	August 2002
POM-POM2/CELLULOSE SYNTHASE INTERACTING1 Is Essential for the Functional Association of Cellulose Synthase and Microtubules in Arabidopsis Bringmann, Martin; Li, Eryang; Sampathkumar, Arun The Plant Cell, Vol. 24, Issue 1 https://doi.org/10.1105/tpc.111.093575	journal	January 2012
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
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
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures Murashige, Toshio; Skoog, Folke Physiologia Plantarum, Vol. 15, Issue 3, p. 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x	journal	July 1962
Failure of Composite Materials Daniel, I. M. Strain, Vol. 43, Issue 1 https://doi.org/10.1111/j.1475-1305.2007.00302.x	journal	February 2007
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
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
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
Tracheary Element Differentiation Turner, Simon; Gallois, Patrick; Brown, David Annual Review of Plant Biology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105236	journal	June 2007
Cellulose Synthesis in Higher Plants Somerville, Chris Annual Review of Cell and Developmental Biology, Vol. 22, Issue 1 https://doi.org/10.1146/annurev.cellbio.22.022206.160206	journal	November 2006
Measuring the distribution of cellulose microfibril angles in primary cell walls by small angle X-ray scattering Saxe, Friederike; Eder, Michaela; Benecke, Gunthard Plant Methods, Vol. 10, Issue 1 https://doi.org/10.1186/1746-4811-10-25	journal	January 2014
The impact of alterations in lignin deposition on cellulose organization of the plant cell wall Liu, Jiliang; Kim, Jeong Im; Cusumano, Joanne C. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0540-z	journal	June 2016

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