Cellulose-pectin spatial contacts are Inherent to never-dried Arabidopsis primary cell walls: Evidence from solid-state nuclear magnetic resonance

Plant Physiology

Volumn 168, Issue 3, 2015, Pages 871-884

  Wang, Tuo ^a   Park, Yong Bum ^b   Cosgrove, Daniel J ^b   Hong, Mei ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

CELLULOSE; PECTIN; POLYGALACTURONIC ACID; WATER;

ARABIDOPSIS; CARBON NUCLEAR MAGNETIC RESONANCE; CELL WALL; CHEMISTRY; CYTOLOGY; DESICCATION; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTON NUCLEAR MAGNETIC RESONANCE; TIME FACTOR;

ARABIDOPSIS; CARBON-13 MAGNETIC RESONANCE SPECTROSCOPY; CELL WALL; CELLULOSE; DESICCATION; MAGNETIC RESONANCE SPECTROSCOPY; PECTINS; PROTON MAGNETIC RESONANCE SPECTROSCOPY; TIME FACTORS; WATER;

EID: 84936133596     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00665     Document Type: Article

References (53)

1. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2011) Plant Cell Walls. Garland Science, New York
2. Atalla RH, Vanderhart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 223: 283-285
3. Bielecki A, Kolbert AC, Levitt MH (1989) Frequency-switched pulse sequences: homonuclear decoupling and dilute spin NMR in solids. Chem Phys Lett 155: 341-346
4. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344: 1879-1900
5. 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 J 3: 1-30
6. Chanliaud E, Gidley MJ (1999) In vitro synthesis and properties of pectin/ Acetobacter xylinus cellulose composites. Plant J 20: 25-35
7. Cornuault V, Manfield IW, Ralet MC, Knox JP (2014) Epitope detection chromatography: a method to dissect the structural heterogeneity and inter-connections of plant cell-wall matrix glycans. Plant J 78: 715-722
8. Cosgrove DJ (2001) Wall structure and wall loosening: a look backwards and forwards. Plant Physiol 125: 131-134
9. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850-861
10. Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22: 122-131
11. 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. Magn Reson Chem 50: 539-550
12. Dick-Perez M, Zhang Y, 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
13. Fleischer A, O’Neill MA, Ehwald R (1999) The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiol 121: 829-838
14. Foster TJ, Ablett S, McCann MC, Gidley MJ (1996) Mobility-resolved C-13-NMR spectroscopy of primary plant cell walls. Biopolymers 39: 51-66
15. Gibeaut DM, Pauly M, Bacic A, Fincher GB (2005) Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta 221: 729-738
16. Goodneratne J, Needs PW, Ryden P, Selvendran RR (1994) Structural features of cell wall polysaccharides from the cotyledons of mung bean Vigna radiata. Carbohydr Res 265: 61-77.
17. Hayashi T, Marsden MP, Delmer DP (1987) Pea xyloglucan and cellulose. VI. Xyloglucan-cellulose interactions in vitro and in vivo. Plant Physiol 83: 384-389
18. Huster D, Xiao L, Hong M (2001) Solid-state NMR investigation of the dynamics of the soluble and membrane-bound colicin Ia channel-forming domain. Biochemistry 40: 7662-7674
19. Ishii T, Matsunaga T (1996) Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp. Carbohydr Res 284: 1-9
20. Jarvis MC (1992) Self-assembly of plant-cell walls. Plant Cell Environ 15: 1-5
21. 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
22. Li S, Su Y, Luo W, Hong M (2010) Water-protein interactions of an arginine-rich membrane peptide in lipid bilayers investigated by solidstate nuclear magnetic resonance spectroscopy. J Phys Chem B 114: 4063-4069
23. Matthews JF, Skopec CE, Mason PE, Zuccato P, Torget RW, Sugiyama J, Himmel ME, Brady JW (2006) Computer simulation studies of micro-crystalline cellulose Ibeta. Carbohydr Res 341: 138-152
24. McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. J Cell Sci 96: 323-334
25. Munowitz MG, Griffin RG, Bodenhausen G, Huang TH (1981) Two-dimensional rotational spin-echo NMR in solids: correlation of chemical shift and dipolar interactions. J Am Chem Soc 103: 2529-2533
26. 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 Physiol 111: 475-485
27. Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Ibeta from synchrotron x-ray and neutron fiber diffraction. J Am Chem Soc 124: 9074-9082
28. Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose I(alpha) from synchrotron x-ray and neutron fiber diffraction. J Am Chem Soc 125: 14300-14306
29. Oehme DP, Downton MT, Doblin MS, Wagner J, Gidley MJ, Bacic A (2015) Unique aspects of the structure and dynamics of elementary Iß cellulose microfibrils revealed by computational simulations. Plant Physiol 168: 3-17
30. Park YB, Cosgrove DJ (2012a) Changes in cell wall biomechanical properties in the xyloglucan-deficient xxtl/xxt2 mutant of Arabidopsis. Plant Physiol 158: 465-475
31. Park YB, Cosgrove DJ (2012b) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specificendo-glucanases. Plant Physiol 158: 1933-1943
32. Peaucelle A, Braybrook S, Höfte H (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci 3: 121
33. Popper ZA, Fry SC (2008) Xyloglucan-pectin linkages are formed intra-protoplasmically, contribute to wall-assembly, and remain stable in the cell wall. Planta 227: 781-794
34. Rienstra CM, Tucker-Kellogg L, Jaroniec CP, Hohwy M, Reif B, McMahon MT, Tidor B, Lozano-Perez T, Griffin RG (2002) De novo determination of peptide structure with solid-state magic-angle spinning NMR spectroscopy. Proc Natl Acad Sci USA 99: 10260-10265
35. Ryden P, Selvendran RR (1990) Structural features of cell-wall polysac-charides of potato (Solanum tuberosum). Carbohydr Res 195: 257-272
36. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, et al (2004) Toward a systems approach to understanding plant cell walls. Science 306: 2206-2211
37. Talbott LD, Ray PM (1992) Molecular size and separability features of pea cell wall polysaccharides: implications for models of primary wall structure. Plant Physiol 98: 357-368
38. Tan L, Eberhard S, Pattathil S, Warder C, Glushka J, Yuan C, Hao Z, Zhu X, Avci U, Miller JS, et al (2013) An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinoga-lactan protein. Plant Cell 25: 270-287
39. Torchia DA (1978) Measurement of proton-enhanced 13CT1 values by a method which suppresses artifacts. J Magn Reson 30: 613-616
40. van Rossum BJ, de Groot CP, Ladizhansky V, Vega S, de Groot HJ (2000) A method for measuring heteronuclear 1H-13C distances in high speed MAS NMR. J Am Chem Soc 122: 3465-3472
41. Wang T, Park YB, Caporini MA, Rosay M, Zhong L, Cosgrove DJ, Hong M (2013) Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc Natl Acad Sci USA 110: 16444-16449
42. Wang T, Salazar A, Zabotina OA, Hong M (2014) Structure and dynamics of Brachypodium primary cell wall polysaccharides from two-dimensional 13C solid-state nuclear magnetic resonance spectroscopy. Biochemistry 53: 2840-2854
43. Wang T, Williams JK, Schmidt-Rohr K, Hong M (2015) Relaxation-compensated difference spin diffusion NMR for detecting 13C-13C long-range correlations in proteins and polysaccharides. J Biomol NMR 61: 97-107
44. Wang T, Zabotina O, Hong M (2012) Pectin-cellulose interactions in the Ara-bidopsis primary cell wall from two-dimensional magic-angle-spinning solidstate nuclear magnetic resonance. Biochemistry 51: 9846-9856
45. White PB, Wang T, Park YB, Cosgrove DJ, Hong M (2014) Water-polysaccharide interactions in the primary cell wall of Arabidopsis thaliana frompolarizationtransfersolid-stateNMR. JAmChemSoc136:10399-10409
46. Yao XL, Hong M (2001) Dipolar filtered 1H-13C heteronuclear correlation spectroscopy for resonance assignment of proteins. J Biomol NMR 20: 263-274
47. Yao XL, Schmidt-Rohr K, Hong M (2001) Medium-and long-distance 1H-13C heteronuclear correlation NMR in solids. J Magn Reson 149:139-143
48. Zablackis E, Huang J, Müller B, Darvill AG, Albersheim P (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107: 1129-1138
49. Zhang T, Mahgsoudy-Louyeh S, Tittmann B, Cosgrove DJ (2014) Visualization of the nanoscale pattern of recently-deposited cellulose mi-crofibrils and matrix materials in never-dried primary walls of the onion epidermis. Cellulose 21: 853-862
50. Zhao Z, Crespi VH, Kubicki JD, Cosgrove DJ, Zhong LH (2014) Molecular dynamics simulation study of xyloglucan adsorption on cellulose surfaces: effects of surface hydrophobicity and side-chain variation. Cellulose 21: 1025-1039
51. Zykwinska A, Thibault JF, Ralet MC (2007) Organization of pectic ara-binan and galactan side chains in association with cellulose microfibrils in primary cell walls and related models envisaged. J Exp Bot 58: 1795-1802
52. Zykwinska A, Thibault JF, Ralet MC (2008) Competitive binding of pectin and xyloglucan with primary cell wall cellulose. Carbohydr Polym 74: 957-961
53. Zykwinska AW, Ralet MCJ, Garnier CD, Thibault JF (2005) Evidence for in vitro binding of pectin side chains to cellulose. Plant Physiol 139: 397-407