Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR

Nature Communications

Volumn 7, Issue , 2016, Pages

  Simmons, Thomas J ^a   Mortimer, Jenny C ^a,d   Bernardinelli, Oigres D ^a,b,c,e   Pöppler, Ann Christin ^c   Brown, Steven P ^c   DeAzevedo, Eduardo R ^b   Dupree, Ray ^c   Dupree, Paul ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE; XYLAN; CARBON;

BIOMASS; CELL ORGANELLE; CELLULOSE; DIGESTIBILITY; MOLECULAR ANALYSIS; NUCLEAR MAGNETIC RESONANCE; ORGANIC COMPOUND; POLYSACCHARIDE;

ARABIDOPSIS; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL WALL; COMPUTER MODEL; CONFORMATION; CONTROLLED STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLANT CELL; PLANT FIBER; PREDICTION; PROTON NUCLEAR MAGNETIC RESONANCE; RIGIDITY; SOLID STATE; CARBOHYDRATE ANALYSIS; CHEMISTRY; GENETICS; MUTATION; PLANT STEM; PROCEDURES;

ARABIDOPSIS;

ARABIDOPSIS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CARBON ISOTOPES; CELL WALL; CELLULOSE; MAGNETIC RESONANCE SPECTROSCOPY; MUTATION; PLANT CELLS; PLANT STEMS; XYLANS;

EID: 85006867360     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13902     Document Type: Article

References (50)

1. Perlack, R. D. & Stokes, B. J., Leads. U.S. Billion-Ton Update: Biomass Supply for a Bioenergy and Bioproducts Industry. Technical Report ORNL/TM-2011/224, 227. (U.S. Department of Energy, Oak Ridge National Laboratory, Oak Ridge, TN, 2011).
2. Carpita, N. & McCann, M. in Biochemistry and Molecular Biology of Plants, Vol. 61 (eds Buchanan, B. B., Wilhelm, G., and Jones, R. L.) 52-108, (American Society of Plant Physiologists, Rockville, IL, 2000).
3. Scheller, H. V. & Ulvskov, P. Hemicelluloses. Annu. Rev. Plant Biol. 61, 263-289 (2010).
4. Atalla, R. H. & Vanderhart, D. L. Native cellulose - a composite of 2 distinct crystalline forms. Science 223, 283-285 (1984).
5. Nishiyama, Y., Langan, P. & Chanzy, H. Crystal structure and hydrogenbonding system in cellulose 1β from synchrotron X-ray and neutron fiber diffraction. J. Am. Chem. Soc. 124, 9074-9082 (2002).
6. Nishiyama, Y., Sugiyama, J., Chanzy, H. & Langan, P. Crystal structure and hydrogen bonding system in cellulose 1α, from synchrotron X-ray and neutron fiber diffraction. J. Am. Chem. Soc. 125, 14300-14306 (2003).
7. Cosgrove, D. J. & Jarvis, M. C. Comparative structure and biomechanics of plant primary and secondary cell walls. Front. Plant Sci. 3, 1-6 (2012).
8. Dick-Perez, M. et al. Structure and Interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solidstate NMR. Biochemistry 50, 989-1000 (2011).
9. Dick-Perez, M., Wang, T., Salazar, A., Zabotina, O. A. & Hong, M. Multidimensional solid-state NMR studies of the structure and dynamics of pectic polysaccharides in uniformly C-13-labeled Arabidopsis primary cell walls. Magn. Reson. Chem. 50, 539-550 (2012).
10. 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 51, 9846-9856 (2012).
11. Wang, T. et al. Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls. Proc. Natl Acad. Sci. USA 110, 16444-16449 (2013).
12. 13C solid-state nuclear magnetic resonance spectroscopy. Biochemistry 53, 2840-2854 (2014).
13. Wang, T., Yang, H., Kubicki, J. D. & Hong, M. Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D Solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules 17, 2210-2222 (2016).
14. 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. J. Exp. Bot. 55, 571-583 (2004).
15. Wu, A. M. et al. The Arabidopsis IRX10 and IRX10-LIKE glycosyltransferases are critical for glucuronoxylan biosynthesis during secondary cell wall formation. Plant J. 57, 718-731 (2009).
16. Brown, D. M. et al. Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J. 52, 1154-1168 (2007).
17. Li, L., Perre, P., Frank, X. & Mazeau, K. A coarse-grain force-field for xylan and its interaction with cellulose. Carbohyd. Polym. 127, 438-450 (2015).
18. Mikkelsen, D., Flanagan, B. M., Wilson, S. M., Bacic, A. & Gidley, M. J. Interactions of arabinoxylan and (1,3)(1,4)-β-glucan with cellulose networks. Biomacromolecules 16, 1232-1239 (2015).
19. Busse-Wicher, M. et al. The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana. Plant J. 79, 492-506 (2014).
20. Busse-Wicher, M., Grantham, N. J., Lyczakowski, J. J., Nikolovski, N. & Dupree, P. Xylan decoration patterns and the plant secondary cell wall molecular architecture. Biochem. Soc. Trans. 44, 74-78 (2016).
21. Bromley, J. R. et al. GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J. 74, 423-434 (2013).
22. Busse-Wicher, M. et al. Evolution of xylan substitution patterns in gymnosperms and angiosperms: implications for xylan interaction with cellulose. Plant Physiol. 171, 2418-2431 (2016).
23. Nieduszynski, I. & Marchessault, R. H. Structure of β-D-(1-4′)Xylan Hydrate. Nature 232, 1335-1344 (1971).
24. 13C-enriched wood. Solid State Nucl. Magn. Reson. 8, 25-32 (1997).
25. Lesage, A., Bardet, M. & Emsley, L. Through-bond carbon-carbon connectivities in disordered solids by NMR. J. Am. Chem. Soc. 121, 10987-10993 (1999).
26. Komatsu, T. & Kikuchi, J. Selective signal detection in solid-state NMR Using rotor-synchronized dipolar dephasing for the analysis of hemicellulose in lignocellulosic biomass. J. Phys. Chem. Lett. 4, 2279-2283 (2013).
27. 13C NMR. Carbohyd. Res. 275, 131-145 (1995).
28. 13C solid state nuclear magnetic resonance spectroscopy. Biochemistry 54, 2335-2345 (2015).
29. Lesage, A., Auger, C., Caldarelli, S. & Emsley, L. Determination of throughbond carbon-carbon connectivities in solid-state NMR using the INADEQUATE experiment. J. Am. Chem. Soc. 119, 7867-7868 (1997).
30. Fayon, F. et al. Through-space contributions to two-dimensional doublequantum J correlation NMR spectra of magic-angle-spinning solids. J. Chem. Phys. 122, 14931 (2005).
31. Pickard, C. J. & Mauri, F. All-electron magnetic response with pseudopotentials: NMR chemical shifts. Phys. Rev. B 63, 245101 (2001).
32. Yates, J. R., Pickard, C. J. & Mauri, F. Calculation of NMR chemical shifts for extended systems using ultrasoft pseudopotentials. Phys. Rev. B 76, 024401 (2007).
33. 13C NMR spectroscopy. Carbohyd. Res. 312, 123-129 (1998).
34. Larsson, P. T., Hult, E. L., Wickholm, K., Pettersson, E. & Iversen, T. CP/MAS C-13-NMR spectroscopy applied to structure and interaction studies on cellulose I. Solid State Nucl. Magn. Reson. 15, 31-40 (1999).
35. Teleman, A., Larsson, P. T. & Iversen, T. On the accessibility and structure of xylan in birch kraft pulp. Cellulose 8, 209-215 (2001).
36. Habibi, Y., Heux, L., Mahrouz, M. & Vignon, M. R. Morphological and structural study of seed pericarp of Opuntia ficus-indica prickly pear fruits. Carbohyd. Polym. 72, 102-112 (2008).
37. Ha, M. A. et al. Structure of cellulose-deficient secondary cell walls from the irx3 mutant of Arabidopsis thaliana. Phytochemistry 61, 7-14 (2002).
38. Brown, D. M., Zeef, L. A. H., Ellis, J., Goodacre, R. & Turner, S. R. Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17, 2281-2295 (2005).
39. 1H dipolar-assisted rotational resonance in magic-angle spinning NMR. Chem. Phys. Lett. 344, 631-637 (2001).
40. 13C long-range correlations in proteins and polysaccharides. J. Biomol. NMR 61, 97-107 (2015).
41. Munowitz, M. G., Griffin, R. G., Bodenhausen, G. & Huang, T. H. Two-dimensional rotational spin-echo nuclear magnetic-resonance in solids-correlation of chemical-shift and dipolar interactions. J. Am. Chem. Soc. 103, 2529-2533 (1981).
42. Pauly, M. & Keegstra, K. Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J. 54, 559-568 (2008).
43. 13C-carbon dioxide - an in vivo labeling system for proteomics and metabolomics research. Proteome Sci. 9, 9 (2011).
44. Clark, S. J. et al. First principles methods using CASTEP. Z. Kristallogr 220, 567-570 (2005).
45. Perdew, J. P., Burke, K. & Ernzerhof, M. Generalized gradient approximation made simple. Phys. Rev. Lett. 77, 3865-3868 (1996).
46. Metz, G., Wu, X. L. & Smith, S. O. Ramped-amplitude cross-polarization in magic-angle-spinning NMR. J. Magn. Reson. Ser. A 110, 219-227 (1994).
47. Fung, B. M., Khitrin, A. K. & Ermolaev, K. An improved broadband decoupling sequence for liquid crystals and solids. J. Magn. Reson. 142, 97-101 (2000).
48. Bielecki, A., Kolbert, A. C. & Levitt, M. H. Frequency-switched pulse sequences-homonuclear decoupling and dilute spin NMR in solids. Chem. Phys. Lett. 155, 341-346 (1989).
49. Terao, T., Miura, H. & Saika, A. Dipolar SASS NMR-spectroscopy - separation of heteronuclear dipolar powder patterns in rotating solids. J. Chem. Phys. 85, 3816-3826 (1986).
50. DeAzevedo, E. R. et al. Intermediate motions as studied by solid-state separated local field NMR experiments. J. Chem. Phys. 128, 128-139 (2008).