Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls

Journal of Experimental Botany

Volumn 67, Issue 2, 2016, Pages 503-514

  Wang, Tuo ^a   Hong, Mei ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Arabidopsis; Brachypodium; cellulose microfibrils; dynamics; intermolecular contact; multidimensional correlation NMR

Indexed keywords

CELLULOSE; HEMICELLULOSE; PECTIN; PLANT PROTEIN; POLYSACCHARIDE;

ARABIDOPSIS; BRACHYPODIUM; CELL WALL; CHEMISTRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

ARABIDOPSIS; BRACHYPODIUM; CELL WALL; CELLULOSE; MAGNETIC RESONANCE SPECTROSCOPY; PECTINS; PLANT PROTEINS; POLYSACCHARIDES;

EID: 84959909269     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv416     Document Type: Review

References (69)

1. Atalla RH, Vander Hart DL. (1984). Native cellulose: a composite of two distinct crystalline forms. Science 223, 283-285
2. Atalla RH, VanderHart DL. (1999). The role of solid state 13C NMR spectroscopy in studies of the nature of native celluloses. Solid State Nuclear Magnetic Resonance 15, 1-19
3. Bardet M, Emsley L, Vincendon M. (1997). Two-dimensional spinexchange solid-state NMR studies of 13 C-enriched wood. Solid State Nuclear Magnetic Resonance 8, 25-32
4. Bax A, Freeman R, Kempsell SP. (1980). Natural abundance 13C-13C coupling observed via double-quantum coherence. Journal of the Amercian Chemical Society 102, 4849-4851
5. Bootten TJ, Harris PJ, Melton LD, Newman RH. (2004). Solid-state 13C-NMR spectroscopy shows that the xyloglucans in the primary cell walls of mung bean (Vigna radiata L) occur in different domains: a new model for xyloglucan-cellulose interactions in the cell wall. Journal of Experimental Botany 55, 571-583
6. Brabham C, Lei L, Gu Y, Stork J, Barrett M, DeBolt S. (2014). Indaziflam herbicidal action: a potent cellulose biosynthesis inhibitor. Plant Physiology 166, 1177-1185
7. Caffall KH, Mohnen D. (2009). The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydrate Research 344, 1879-1900
8. Carpita NC. (1983). Hemicellulosic polymers of cell walls of Zea coleoptiles. Plant Physiology 72, 515-521
9. Carpita NC, Gibeaut DM. (1993). Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant Journal 3, 1-30
10. Carpita NC. (1996). Structure and biogenesis of the cell walls of grasses. Annual Review of Plant Physiology and Plant Molecular Biology 47, 445-476
11. Cavalier DM, Lerouxel O, Neumetzler L, et al. (2008). Disrupting Two Arabidopsis thaliana Xylosyltransferase Genes Results in Plants Deficient in Xyloglucan, a Major Primary Cell Wall Component. Plant Cell 20, 1519-1537
12. Cegelski L, O?Connor RD, Stueber D, Singh M, Poliks B, Schaefer J. (2010). Plant Cell-Wall Cross-Links by REDOR NMR Spectroscopy. Journal of the Amercian Chemical Society 132, 16052-16057
13. Cosgrove DJ. (2001). Wall structure and wall loosening. A look backwards and forwards. Plant Physiology 125, 131-134
14. Cosgrove DJ. (2005). Growth of the plant cell wall. Nature Reviews Molecular Cell Biology 6, 850-861
15. Cosgrove DJ. (2014). Re-constructing our models of cellulose and primary cell wall assembly. Current Opinion in Plant Biology 22C, 122-131
16. Dick-Perez M, Zhang YA, Hayes J, Salazar A, Zabotina OA, Hong M. (2011). Structure and interactions of plant cell wall polysaccharides by two-and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50, 989-1000
17. Dick-Perez M, Wang T, Salazar A, Zabotina OA, Hong M. (2012). Multidimensional solid-state NMR studies of the structure and dynamics of pectic polysaccharides in uniformly 13C-labeled Arabidopsis primary cell walls. Magnetic Resonance in Chemistry 50, 539-550
18. Dupree R, Simmons TJ, Mortimer JC, Patel D, Iuga D, Brown SP, Dupree P. (2015). Probing the Molecular Architecture of Arabidopsis thaliana Secondary Cell Walls Using Two-and Three-Dimensional 13C Solid State Nuclear Magnetic Resonance Spectroscopy. Biochemistry 54, 2335-2345
19. Earl WL, VanderHart DL. (1981). Observations by High-Resolution Carbon-13 Nuclear Magnetic Resonance of Cellulose I Related to Morphology and Crystal Structure. Macromolecules 14, 570-574
20. Endler A, Persson S. (2011). Cellulose Synthases and Synthesis in Arabidopsis. Mol. Plant 4, 199-211
21. Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC. (2011). Nanostructure of cellulose microfibrils in spruce wood. Proceedings of the National Academy of Sciences of the United States of America 108, E1195-E1203
22. Fry SC. (1989). The structure and functions of xyloglucan. Journal of Experimental Botany 40, 1-11
23. Guerriero G, Fugelstad J, Bulone V. (2010). What do we really know about cellulose biosynthesis in higher plants? Journal of Integrative Plant Biology 52, 161-175
24. Harris DM, Corbin K, Wang T, et al. (2012). Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1A903V and CESA3T942I of cellulose synthase. Proceedings of the National Academy of Sciences of the United States of America 109, 4098-4103
25. Hediger S, Emsley L, Fischer M. (1999). Solid-state NMR characterization of hydration effects on polymer mobility in onion cell-wall material. Carbohydrate Research 322, 102-112
26. Hediger S, Lesage A, Emsley L. (2002). A new NMR method for the study of local mobility in solids and application to hydration of biopolymers in plant cell walls. Macromolecules 35, 5078-5084
27. Herth W. (1983). Arrays of plasma-membrane rosettes involved in cellulose microfibril formation of Spirogyra. Planta 159, 347-356
28. Hill JLJ, Hammudi MB, Tien M. (2014). The Arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. Plant Cell 26, 4834-4842
29. Hohwy M, Rienstra CM, Jaroniec CP, Griffin RG. (1999). Fivefold symmetric homonuclear dipolar recoupling in rotating solids: Application to double quantum spectroscopy. Journal of Chemical Physics 110, 7983-7992
30. Horii F, Hirai A, Kitamaru R. (1987). CP/MAS C-13 NMR spectra of the crystalline components of native celluloses. Macromolecules 20, 2117-2120
31. Jarvis M. (2003). Chemistry: cellulose stacks up. Nature 426, 611-612
32. Jarvis MC. (1992). Self-assembly of plant cell walls. Plant Cell and Environment 15, 1-5
33. Johnson RL, Schmidt-Rohr K. (2014). Quantitative solid-state 13C NMR with signal enhancement by multiple cross polarization. Journal of Magnetic Resonance 239, 44-49
34. Kennedy CJ, Cameron GJ, Sturcova A, Apperley DC, Altaner C, Wess TJ, Jarvis MC. (2007). Microfibril diameter in celery collenchyma cellulose: X-ray scattering and NMR evidence. Cellulose 14, 235-246
35. Kiemle SN, Zhang X, Esker AR, Toriz G, Gatenholm P, Cosgrove DJ. (2014). Role of (1, 3)(1, 4)-β-glucan in cell walls: interaction with cellulose. Biomacromolecules 15, 1727-1736
36. Komatsu T, Kikuchi J. (2013). Selective Signal Detection in Solid-State NMR Using Rotor-Synchronized Dipolar Dephasing for the Analysis of Hemicellulose in Lignocellulosic Biomass. Journal of Physical Chemistry Letters 4, 2279-2283
37. Kono H, Erata T, Takai M. (2003). Determination of the through-bond carbon-carbon and carbon-proton connectivities of the native celluloses in the solid state. Macromolecules 36, 5131-5138
38. Kono H, Numata Y. (2006). Structural investigation of cellulose Ia and Iβ by 2D RFDR NMR spectroscopy: determination of sequence of magnetically inequivalent D-glucose units along cellulose chain. Cellulose 13, 317-326
39. Larsson PT, Hult EL, Wickholm K, Pettersson E, Iversen T. (1999). CP/MAS 13C NMR spectroscopy applied to structure and interaction studies on cellulose I. Solid State Nuclear Magnetic Resonance 15, 31-40
40. Lesage A, Auger C, Caldarelli S, Emsley L. (1997). Determination of through-bond carbon-carbon connectivities in solid-state NMR using the INADEQUATE experiment. Journal of the Amercian Chemical Society 119, 7867-7868
41. Li S, Zhang Y, Hong M. (2010). 3D 13C-13C-13C correlation NMR for de novo distance determination of solid proteins and application to a human alpha-defensin. Journal of Magnetic Resonance 202, 203-210
42. Matthews JF, Skopec CE, Mason PE, Zuccato P, Torget RW, Sugiyama J, Himmel ME, Brady JW. (2006). Computer simulation studies of microcrystalline cellulose Iβ. Carbohydrate Research 341, 138-152
43. Mccann MC, Wells B, Roberts K. (1990). Direct visualization of crosslinks in the primary plant cell wall. Journal of Cell Science 96, 323-334
44. Mccann MC, Roberts K, Wilson RH, Gidley MJ, Gibeaut DM, Kim JB, Carpita NC. (1995). Old and new ways to probe plant cell wall architecture. Canadian Journal of Botany 73, S103-S113
45. Newman RH, Ha MA, Melton LD. (1994). Solid-state 13C NMR investigation of molecular ordering in the cellulose of apple cell walls. Journal of Agricultural and Food Chemistry 42, 1402-1406
46. Newman RH, Davies LM, Harris PJ. (1996). Solid-state 13C nuclear magnetic resonance characterization of cellulose in the cell walls of Arabidopsis thaliana leaves. Plant Physiology 111, 475-485
47. Newman RH, Hill SJ, Harris PJ. (2013). 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 Physiology 163, 1558-1567
48. Nishiyama Y, Langan P, Chanzy H. (2002). Crystal structure and hydrogen-bonding system in cellulose Iβ from synchrotron X-ray and neutron fiber diffraction. Journal of the Amercian Chemical Society 124, 9074-9082
49. Nishiyama Y, Kim UJ, Kim DY, Katsumata KS, May RP, Langan P. (2003a). Periodic disorder along ramie cellulose microfibrils. Biomacromolecules 4, 1013-1017
50. Nishiyama Y, Sugiyama J, Chanzy H, Langan P. (2003b). Crystal structure and hydrogen bonding system in cellulose Ia, from synchrotron X-ray and neutron fiber diffraction. Journal of the Amercian Chemical Society 125, 14300-14306
51. Park YB, Cosgrove DJ. (2012a). Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of arabidopsis. Plant Physiology 158, 465-475
52. Park YB, Cosgrove DJ. (2012b). A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiology 158, 1933-1943
53. Park YB, Cosgrove DJ. (2015). Xyloglucan and its interactions with other components of the growing cell wall. Plant and Cell Physiology. 56, 180-194
54. Scheible WR, Eshed R, Richmond T, Delmer DP, Somerville C. (2001). Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proceedings of the National Academy of Sciences of the United States of America 98, 10079-10084
55. Sethaphong L, Haigler CH, Kubicki JD, Zimmer J, Bonetta D, DeBolt S, Yingling YG. (2013). Tertiary model of a plant cellulose synthase. Proceedings of the National Academy of Sciences of the United States of America 110, 7512-7517
56. Takegoshi K, Nakamura S, Terao T. (2001). 13C-1H dipolar-assisted rotational resonance in magic-angle spinning NMR. Chemical. Physics Letters 344, 631-637
57. Talbott LD, Ray PM. (1992). Molecular-size and separability features of Pea cell wall polysaccharides. Implications for models of primary wall structure. Plant Physiology 98, 357-368
58. Taylor NG. (2008). Cellulose biosynthesis and deposition in higher plants. New Phytologist 178, 239-252
59. Thomas LH, Forsyth VT, Sturcova A, Kennedy CJ, May RP, Altaner CM, Apperley DC, Wess TJ, Jarvis MC. (2013). Structure of cellulose microfibrils in primary cell walls from Collenchyma. Plant Physiology 161, 465-476
60. Vietor RJ, Newman RH, Ha MA, Apperley DC, Jarvis MC. (2002). Conformational features of crystal-surface cellulose from higher plants. Plant Journal 30, 721-731
61. Vogel J. (2008). Unique aspects of the grass cell wall. Current Opinion in Plant Biology 11, 301-307
62. Wang T, Zabotina O, Hong M. (2012). Pectin-cellulose interactions in the Arabidopsis primary cell wall from two-dimensional magic-anglespinning solid-state nuclear magnetic resonance. Biochemistry 51, 9846-9856
63. Wang T, Park YB, Caporini MA, Rosay M, Zhong LH, Cosgrove DJ, Hong M. (2013). Sensitivity-enhanced solid-state NMR detection of expansin?s target in plant cell walls. Proceedings of the National Academy of Sciences of the United States of America 110, 16444-16449
64. Wang T, Salazar A, Zabotina OA, Hong M. (2014). Structure and dynamics of Brachypodium primary cell wall polysaccharides from twodimensional 13C solid-state nuclear magnetic resonance spectroscopy. Biochemistry 53, 2840-2854
65. Wang T, Park YB, Cosgrove DJ, Hong M. (2015a). Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis thaliana Primary Cell Walls: Evidence from Solid-State NMR. Plant Physiology 168, 871-884
66. Wang T, Williams JK, Schmidt-Rohr K, Hong M. (2015b). Relaxationcompensated difference spin diffusion NMR for detecting 13C-13C long-range correlations in proteins and polysaccharides. Journal of Biomolecular NMR 61, 97-107
67. White PB, Wang T, Park YB, Cosgrove DJ, Hong M. (2014). Waterpolysaccharide interactions in the primary cell wall of Arabidopsis thaliana from polarization transfer solid-state NMR. Journal of the Amercian Chemical Society 136, 10399-10409
68. Woodward JR, Phillips DR, Fincher GB. (1988). Water-soluble (1->3, 1->4)-β-D-glucans from Barley (Hordeum-Vulgare) Endosperm.IV. Comparison of 40°C and 65°C Soluble Fractions. Carbohydrate Polymer 8, 85-97
69. Zykwinska A, Thibault JF, Ralet MC. (2007). Organization of pectic arabinan and galactan side chains in association with cellulose microfibrils in primary cell walls and related models envisaged. Journal of Experimental Botany 58, 1795-1802