Cellulose Structural Polymorphism in Plant Primary Cell Walls Investigated by High-Field 2D Solid-State NMR Spectroscopy and Density Functional Theory Calculations

Biomacromolecules

Volumn 17, Issue 6, 2016, Pages 2210-2222

  Wang, Tuo ^a   Yang, Hui ^b   Kubicki, James D ^c   Hong, Mei ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELLS; CHAINS; CHEMICAL BONDS; CHEMICAL SHIFT; CONFORMATIONS; CYTOLOGY; DENSITY FUNCTIONAL THEORY; HYDROGEN BONDS; IODINE; LIGHT POLARIZATION; MAGIC ANGLE SPINNING; NEUTRON DIFFRACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYSACCHARIDES; SPATIAL DISTRIBUTION;

CELLULOSE STRUCTURES; MATRIX POLYSACCHARIDES; POLYMORPHIC STRUCTURE; PRIMARY WALL CELLULOSE; SOLID-STATE NMR SPECTROSCOPY; SOLID-STATE NUCLEAR MAGNETIC RESONANCE; STRUCTURAL POLYMORPHISMS; X-RAY AND NEUTRON DIFFRACTION;

CELLULOSE;

CARBON 13; CELLULOSE; GLUCOSE; HEMICELLULOSE; POLYSACCHARIDE; CARBON;

ARABIDOPSIS; ARTICLE; BRACHYPODIUM; CELL WALL; CONFORMATION; CRYSTAL STRUCTURE; DENSITY FUNCTIONAL THEORY; HYDROGEN BOND; MAIZE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLANT CELL; PRIMARY CELL; PRIORITY JOURNAL; TORSION; CHEMISTRY; MOLECULAR MODEL; PLANT; QUANTUM THEORY;

ALGAE; BACTERIA; CELLULOSE STRUCTURE; FIBRILS; HYDROGEN BONDS; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE; POLARIZATION;

CARBON ISOTOPES; CELL WALL; CELLULOSE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PLANTS; QUANTUM THEORY;

EID: 84974824141     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/acs.biomac.6b00441     Document Type: Article

References (79)

1. Jarvis, M. Chemistry: cellulose stacks up Nature 2003, 426, 611-612 10.1038/426611a
2. Pauly, M.; Keegstra, K. Cell-wall carbohydrates and their modification as a resource for biofuels Plant J. 2008, 54, 559-568 10.1111/j.1365-313X.2008.03463.x
3. Horii, F.; Hirai, A.; Kitamaru, R. Solid-state high-resolution C-13 NMR studies of regenerated cellulose samples with different crystallites Polym. Bull. 1982, 8, 163-170 10.1007/BF00263023
4. Atalla, R. H.; Vanderhart, D. L. Native cellulose: a composite of two distinct crystalline forms Science 1984, 223, 283-285 10.1126/science.223.4633.283
5. 13C NMR evidence for the coexistence of two crystalline forms in native celluloses ACS Symp. Ser. 1987, 340, 88-118 10.1021/bk-1987-0340.ch005
6. 13C NMR spectrum of the native cellulose J. Am. Chem. Soc. 2002, 124, 7506-7511 10.1021/ja010704o
7. Kono, H.; Erata, T.; Takai, M. Determination of the through-bond carbon-carbon and carbon-proton connectivities of the native celluloses in the solid state Macromolecules 2003, 36, 5131-5138 10.1021/ma021769u
8. β by 2D RFDR NMR spectroscopy: determination of sequence of magnetically inequivalent D-glucose units along cellulose chain Cellulose 2006, 13, 317-326 10.1007/s10570-005-9025-0
9. β from synchrotron X-ray and neutron fiber diffraction J. Am. Chem. Soc. 2002, 124, 9074-9082 10.1021/ja0257319
10. Nishiyama, Y.; Sugiyama, J.; Chanzy, H.; Langan, P. Crystal structure and hydrogen bonding system in cellulose Iα, from synchrotron X-ray and neutron fiber diffraction J. Am. Chem. Soc. 2003, 125, 14300-14306 10.1021/ja037055w
11. Carpita, N. C. Structure and biogenesis of the cell walls of grasses Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47, 445-476 10.1146/annurev.arplant.47.1.445
12. Carpita, N. C.; Gibeaut, D. M. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth Plant J. 1993, 3, 1-30 10.1111/j.1365-313X.1993.tb00007.x
13. Cosgrove, D. J. Re-constructing our models of cellulose and primary cell wall assembly Curr. Opin. Plant Biol. 2014, 22, 122-131 10.1016/j.pbi.2014.11.001
14. Dick-Perez, M.; Zhang, Y. A.; Hayes, J.; Salazar, A.; Zabotina, O. A.; Hong, M. Structure and interactions of plant cell wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR Biochemistry 2011, 50, 989-1000 10.1021/bi101795q
15. 13C-labeled Arabidopsis primary cell walls Magn. Reson. Chem. 2012, 50, 539-550 10.1002/mrc.3836
16. Wang, T.; Zabotina, O.; Hong, M. Pectin-cellulose interactions in the Arabidopsis primary cell wall from two-dimensional magic-angle-spinning solid-state nuclear magnetic resonance Biochemistry 2012, 51, 9846-9856 10.1021/bi3015532
17. 13C solid-state nuclear magnetic resonance spectroscopy Biochemistry 2014, 53, 2840-2854 10.1021/bi500231b
18. Wang, T.; Park, Y. B.; Cosgrove, D. J.; Hong, M. Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis thaliana Primary Cell Walls: Evidence from Solid-State NMR Plant Physiol. 2015, 168, 871 10.1104/pp.15.00665
19. Wang, T.; Hong, M. Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls J. Exp. Bot. 2016, 67, 503-514 10.1093/jxb/erv416
20. 13C long-range correlations in proteins and polysaccharides J. Biomol. NMR 2015, 61, 97-107 10.1007/s10858-014-9889-0
21. Cosgrove, D. J. Growth of the plant cell wall Nat. Rev. Mol. Cell Biol. 2005, 6, 850-861 10.1038/nrm1746
22. Kimura, S.; Laosinchai, W.; Itoh, T.; Cui, X.; Linder, C. R.; Brown, R. M. J. Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant vigna angularis Plant Cell 1999, 11, 2075-2086 10.2307/3871010
23. 13C nuclear magnetic resonance characterization of cellulose in the cell walls of Arabidopsis thaliana leaves Plant Physiol. 1996, 111, 475-485 10.1104/pp.111.2.475
24. Kennedy, C. J.; Cameron, G. J.; Sturcova, A.; Apperley, D. C.; Altaner, C.; Wess, T. J.; Jarvis, M. C. Microfibril diameter in celery collenchyma cellulose: X-ray scattering and NMR evidence Cellulose 2007, 14, 235-246 10.1007/s10570-007-9116-1
25. Fernandes, A. N.; Thomas, L. H.; Altaner, C. M.; Callow, P.; Forsyth, V. T.; Apperley, D. C.; Kennedy, C. J.; Jarvis, M. C. Nanostructure of cellulose microfibrils in spruce wood Proc. Natl. Acad. Sci. U. S. A. 2011, 108, E1195-E1203 10.1073/pnas.1108942108
26. Newman, R. H.; Hill, S. J.; Harris, P. J. Wide-angle x-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls Plant Physiol. 2013, 163, 1558-1567 10.1104/pp.113.228262
27. Thomas, L. H.; Forsyth, V. T.; Sturcova, A.; Kennedy, C. J.; May, R. P.; Altaner, C. M.; Apperley, D. C.; Wess, T. J.; Jarvis, M. C. Structure of cellulose microfibrils in primary cell walls from Collenchyma Plant Physiol. 2013, 161, 465-476 10.1104/pp.112.206359
28. Oehme, D. P.; Downton, M. T.; Doblin, M. S.; Wagner, J.; Gidley, M. J.; Bacic, A. Unique Aspects of the Structure and Dynamics of Elementary Iβ Cellulose Microfibrils Revealed by Computational Simulations Plant Physiol. 2015, 168, 3-U654 10.1104/pp.114.254664
29. Hill, J. L.; Hammudi, M. B.; Tien, M. The Arabidopsis Cellulose Synthase Complex: A Proposed Hexamer of CESA Trimers in an Equimolar Stoichiometry Plant Cell 2014, 26, 4834-4842 10.1105/tpc.114.131193
30. Zhang, T.; Mahgsoudy-Louyeh, S.; Tittmann, B.; Cosgrove, D. J. Visualization of the nanoscale pattern of recently-deposited cellulose microfibrils and matrix materials in never-dried primary walls of the onion epidermis Cellulose 2014, 21, 853-862 10.1007/s10570-013-9996-1
31. Zhang, T.; Zheng, Y.; Cosgrove, D. J. Spatial Organization of Cellulose Microfibrils and Matrix Polysaccharides in Primary Plant Cell Walls as Imaged by Multi-Channel Atomic Force Microscopy Plant J. 2016, 85, 179-192 10.1111/tpj.13102
32. T942I of cellulose synthase Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 4098-4103 10.1073/pnas.1200352109
33. White, P. B.; Wang, T.; Park, Y. B.; Cosgrove, D. J.; Hong, M. Water-polysaccharide interactions in the primary cell wall of Arabidopsis thaliana from polarization transfer solid-state NMR J. Am. Chem. Soc. 2014, 136, 10399-10409 10.1021/ja504108h
34. Bennett, A. E.; Ok, J. H.; Griffin, R. G.; Vega, S. Chemical shift correlation spectroscopy in rotating solids: radiofrequency-driven dipolar recoupling and longitudinal exchange J. Chem. Phys. 1992, 96, 8624-8627 10.1063/1.462267
35. Hong, M.; Griffin, R. G. Resonance Assignment for Solid Peptides by Dipolar-Mediated 13C/15N Correlation Solid-State NMR J. Am. Chem. Soc. 1998, 120, 7113-7114 10.1021/ja980775w
36. Rienstra, C. M.; Hohwy, M.; Hong, M.; Griffin, R. G. 2D and 3D 15N-13C-13C NMR chemical shift correlation spectroscopy of solids: assignment of MAS spectra of peptides J. Am. Chem. Soc. 2000, 122, 10979-10990 10.1021/ja001092v
37. 13C Spin Exchange in Rigid Crystalline Organic-Solids J. Magn. Reson. 1987, 72, 13-47 10.1016/0022-2364(87)90173-9
38. Kubicki, J. D.; Mohamed, M. N. A.; Watts, H. D. Quantum mechanical modeling of the structures, energetics and spectral properties of I alpha and I beta cellulose Cellulose 2013, 20, 9-23 10.1007/s10570-012-9838-6
39. Kubicki, J. D.; Watts, H. D.; Zhao, Z.; Zhong, L. H. Quantum mechanical calculations on cellulose-water interactions: structures, energetics, vibrational frequencies and NMR chemical shifts for surfaces of I alpha and I beta cellulose Cellulose 2014, 21, 909-926 10.1007/s10570-013-0029-x
40. Adamo, C.; Barone, V. Exchange functionals with improved long-range behavior and adiabatic connection methods without adjustable parameters: The mPW and mPW1PW models J. Chem. Phys. 1998, 108, 664-675 10.1063/1.475428
41. Rassolov, V. A.; Ratner, M. A.; Pople, J. A.; Redfern, P. C.; Curtiss, L. A. 6-31G∗ basis set for third-row atoms J. Comput. Chem. 2001, 22, 976-984 10.1002/jcc.1058
42. Wolinski, K.; Hinton, J. F.; Pulay, P. Efficient implementation of the gauge-independent atomic orbital method for NMR chemical shift calculations J. Am. Chem. Soc. 1990, 112, 8251-8260 10.1021/ja00179a005
43. Schreckenbach, G.; Ziegler, T. Calculation of NMR Shielding Tensors Using Gauge-Including Atomic Orbitals and Modern Density Functional Theory J. Phys. Chem. 1995, 99, 606-611 10.1021/j100002a024
44. Cheeseman, J. R.; Trucks, G. W.; Keith, T. A.; Frisch, M. J. A comparison of models for calculating nuclear magnetic resonance shielding tensors J. Chem. Phys. 1996, 104, 5497-5509 10.1063/1.471789
45. Bühl, M.; Kaupp, M.; Malkina, O. L.; Malkin, V. G. The DFT route to NMR chemical shifts J. Comput. Chem. 1999, 20, 91-105 10.1002/(SICI)1096-987X(19990115)20:1<91::AID-JCC10>3.0.CO;2-C
46. 1H Chemical Shifts in Chloroform Solution J. Chem. Theory Comput. 2006, 2, 1085-1092 10.1021/ct6001016
47. 13C Chemical Shifts: A Useful Tool for Natural Product, Mechanistic, and Synthetic Organic Chemistry Chem. Rev. 2012, 112, 1839-1862 10.1021/cr200106v
48. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Montgomery, J. A.; Vreven, T.; Kudin, K. N.; Burant, J. C. et al.; Gaussian 09, revision B.01; Gaussian, Inc.: Wallingford, CT, 2009.
49. 13C NMR Calculations J. Org. Chem. 2009, 74, 7254-7260 10.1021/jo901234h
50. Watts, H. D.; Mohamed, M. N. A.; Kubicki, J. D. Comparison of Multistandard and TMS-Standard Calculated NMR Shifts for Coniferyl Alcohol and Application of the Multistandard Method to Lignin Dimers J. Phys. Chem. B 2011, 115, 1958-1970 10.1021/jp110330q
51. Gottlieb, H. E.; Kotlyar, V.; Nudelman, A. NMR Chemical Shifts of Common Laboratory Solvents as Trace Impurities J. Org. Chem. 1997, 62, 7512-7515 10.1021/jo971176v
52. 13C NMR distinction between categories of molecular order and disorder in cellulose Cellulose 1995, 2, 95-110 10.1007/BF00816383
53. I Macromolecules 2003, 36, 3589-3592 10.1021/ma021015f
54. Yang, Y.; Fritzsching, K. J.; Hong, M. Resonance assignment of the NMR spectra of disordered proteins using a multi-objective non-dominated sorting genetic algorithm J. Biomol. NMR 2013, 57, 281-296 10.1007/s10858-013-9788-9
55. Tycko, R.; Hu, K. N. A Monte Carlo/simulated annealing algorithm for sequential resonance assignment in solid state NMR of uniformly labeled proteins with magic-angle spinning J. Magn. Reson. 2010, 205, 304-314 10.1016/j.jmr.2010.05.013
56. 13C NMR chemical shifts Cellulose 2014, 21, 3979-3991 10.1007/s10570-014-0448-3
57. Cosgrove, D. J. Loosening of plant cell walls by expansins Nature 2000, 407, 321-326 10.1038/35030000
58. Cosgrove, D. J. Wall structure and wall loosening. A look backwards and forwards Plant Physiol. 2001, 125, 131-134 10.1104/pp.125.1.131
59. Wang, T.; Park, Y. B.; Caporini, M. A.; Rosay, M.; Zhong, L. H.; Cosgrove, D. J.; Hong, M. Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 16444-16449 10.1073/pnas.1316290110
60. Donaldson, L. Cellulose microfibril aggregates and their size variation with cell wall type Wood Sci. Technol. 2007, 41, 443-460 10.1007/s00226-006-0121-6
61. 13C NMR study of cellulose structure in spruce wood and kraft pulp Cellulose 2000, 7, 35-55 10.1023/A:1009236932134
62. Hult, E. L.; Larsson, P. T.; Iversen, T. Cellulose fibril aggregation-an inherent property of kraft pulps Polymer 2001, 42, 3309-3314 10.1016/S0032-3861(00)00774-6
63. 13C NMR spectroscopy Carbohydr. Res. 1998, 312, 123-129 10.1016/S0008-6215(98)00236-5
64. Cadars, S.; Lesage, A.; Emsley, L. Chemical shift correlations in disordered solids J. Am. Chem. Soc. 2005, 127, 4466-4476 10.1021/ja043698f
65. Lesage, A.; Bardet, M.; Emsley, L. Through-bond carbon-carbon connectivities in disordered solids by NMR J. Am. Chem. Soc. 1999, 121, 10987-10993 10.1021/ja992272b
66. 13C Solid State Nuclear Magnetic Resonance Spectroscopy Biochemistry 2015, 54, 2335-2345 10.1021/bi501552k
67. Salager, E.; Stein, R. S.; Pickard, C. J.; Elena, B.; Emsley, L. Powder NMR crystallography of thymol Phys. Chem. Chem. Phys. 2009, 11, 2610-2621 10.1039/b821018g
68. 13C NMR chemical shifts of model cellulosic fragments as a function of size Cellulose 2014, 21, 53-70 10.1007/s10570-013-0128-8
69. 13C chemical shift constrained crystal structure refinement of cellulose Iα and its verification by NMR anisotropy experiments Macromolecules 2006, 39, 6125-6132 10.1021/ma052439n
70. 13C heteronuclear correlation spectroscopy for resonance assignment of proteins J. Biomol. NMR 2001, 20, 263-274 10.1023/A:1011251924874
71. 13C heteronuclear correlation NMR in solids J. Magn. Reson. 2001, 149, 139-143 10.1006/jmre.2001.2285
72. Dumez, J. N.; Emsley, L. A master-equation approach to the description of proton-driven spin diffusion from crystal geometry using simulated zero-quantum lineshapes Phys. Chem. Chem. Phys. 2011, 13, 7363-7370 10.1039/c1cp00004g
73. Zhao, Z.; Crespi, V. H.; Kubicki, J. D.; Cosgrove, D. J.; Zhong, L. H. Molecular dynamics simulation study of xyloglucan adsorption on cellulose surfaces: effects of surface hydrophobicity and side-chain variation Cellulose 2014, 21, 1025-1039 10.1007/s10570-013-0041-1
74. Park, Y. B.; Cosgrove, D. J. A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases Plant Physiol. 2012, 158, 1933-1943 10.1104/pp.111.192880
75. Park, Y. B.; Cosgrove, D. J. Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of arabidopsis Plant Physiol. 2012, 158, 465-475 10.1104/pp.111.189779
76. Vietor, R. J.; Newman, R. H.; Ha, M. A.; Apperley, D. C.; Jarvis, M. C. Conformational features of crystal-surface cellulose from higher plants Plant J. 2002, 30, 721 10.1046/j.1365-313X.2002.01327.x
77. Czaja, W. K.; Young, D. J.; Kawecki, M.; Brown, R. M. The future prospects of microbial cellulose in biomedical applications Biomacromolecules 2007, 8, 1-12 10.1021/bm060620d
78. Ross, P.; Mayer, R.; Benziman, M. Cellulose biosynthesis and function in bacteria Microbiol. Rev. 1991, 55, 35-58
79. Klemm, D.; Heublein, B.; Fink, H. P.; Bohn, A. Cellulose: fascinating biopolymer and sustainable raw material Angew. Chem.; Int. Ed. 2005, 44, 3358-3393 10.1002/anie.200460587