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Fast MAS 1H–13C correlation NMR for structural investigations of plant cell walls

  • Pyae Phyo
  • Mei HongEmail author
Article

Abstract

Plant cell walls consist of a mixture of polysaccharides that render the cell wall a strong and dynamic material. Understanding the molecular structure and dynamics of wall polysaccharides is important for understanding and improving the properties of this energy-rich biomaterial. So far, solid-state NMR studies of cell wall structure and dynamics have solely relied on 13C chemical shifts measured from 2D and 3D correlation experiments. To increase the spectral resolution, sensitivity and upper limit of measurable distances, it is of interest to explore 1H chemical shifts and 1H-detected NMR experiments for analyzing cell walls. Here we demonstrate 2D and 3D 1H–13C correlation experiments at both moderate and fast MAS frequencies of 10–50 kHz to resolve and assign 1H chemical shifts of matrix polysaccharides in Arabidopsis primary cell walls. Both 13C-detected and 1H-detected experiments are implemented and are shown to provide useful and complementary information. Using the assigned 1H chemical shifts, we measured long-range correlations between matrix polysaccharides and cellulose using 1H–1H instead of 13C–13C spin diffusion, and the 2D experiments can be conducted with either 13C or 1H detection.

Keywords

Arabidopsis 1H chemical shift Ultrafast MAS 1H detection Cellulose Matrix polysaccharides 

Abbreviations

Ara

Arabinose

CW

Cell wall

CP

Cross polarization

DP

Direct polarization

Gal

Galactose

GalA

Galacturonic acid

Glc

Glucose

HG

Homogalacturonan

INEPT

Insensitive Nuclei Enhanced by Polarization Transfer

i

Interior crystalline cellulose

MurNac

N-Acetyl-muramic acid

Man

Mannose

MAS

Magic-angle spinning

RG-I

Rhamnogalacturonan I

Rha

Rhamnose

SSNMR

Solid-state nuclear magnetic resonance

s

Surface amorphous cellulose

TOCSY

TOtal Correlated SpectroscopY

XyG

Xyloglucan

Xyl

Xylose

Xn

Xylan

Notes

Acknowledgements

This research was supported by the Center for Lignocellulose Structure and Formation, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Basic Energy Sciences under Award # DE-SC0001090.

References

  1. Agarwal V, Reif B (2008) Residual methyl protonation in perdeuterated proteins for multi-dimensional correlation experiments in MAS solid-state NMR spectroscopy. J Magn Reson 194:16–24ADSCrossRefGoogle Scholar
  2. Andreas LB et al (2016) Structure of fully protonated proteins by proton-detected magic-angle spinning NMR. Proc Natl Acad Sci USA 113:9187–9192CrossRefGoogle Scholar
  3. Baldus M, Meier BH (1996) Total correlation spectroscopy in the solid state. The use of scalar couplings to determine the through-bond connectivity. J Magn Reson A 121:65–69ADSCrossRefGoogle Scholar
  4. Bax A, Clore GM, Gronenborn AM (1990) 1H-1H correlation via isotropic mixing of 13C magnetization, a new 3-dimensional approach for assigning 1H and 13C spectra of 13C-enriched proteins. J Magn Reson 88:425–431ADSGoogle Scholar
  5. Bennett AE, Rienstra CM, Griffiths JM, Zhen WG, Lansbury PT, Griffin RG (1998) Homonuclear radio frequency-driven recoupling in rotating solids. J Chem Phys 108:9463–9479ADSCrossRefGoogle Scholar
  6. Bielecki A, Kolbert AC, Levitt MH (1989) Frequency-switched pulse sequences—homonuclear decoupling and dilute spin NMR in solids. Chem Phys Lett 155:341–346ADSCrossRefGoogle Scholar
  7. Bougault C, Ayala I, Vollmer W, Simorre JP, Schanda P (2019) Studying intact bacterial peptidoglycan by proton-detected NMR spectroscopy at 100 kHz MAS frequency. J Struct Biol 206:66–72CrossRefGoogle Scholar
  8. Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900CrossRefGoogle Scholar
  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 J 3:1–30CrossRefGoogle Scholar
  10. Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22C:122–131CrossRefGoogle Scholar
  11. Cosgrove DJ, Jarvis MC (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3:204CrossRefGoogle Scholar
  12. D’Auria M, Paloma LG, Minale L, Riccio R (1992) Structure chacterization by two-dimensional NMR spectroscopy, of two marine triterpene oligoglycosides from a pacific sponge of the genus Erylus. Tetrahedron 48:491–498CrossRefGoogle Scholar
  13. 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 50:989–1000CrossRefGoogle Scholar
  14. 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 50:539–550CrossRefGoogle Scholar
  15. Dregni AJ et al (2019) In vitro 0N4R tau fibrils contain a monomorphic b-sheet core enclosed by dynamically heterogeneous fuzzy coat segments. Proc Natl Acad Sci USA 116:16357–16366CrossRefGoogle Scholar
  16. 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 54:2335–2345CrossRefGoogle Scholar
  17. Elena B, Lesage A, Steuernagel S, Bockmann A, Emsley L (2005) Proton to carbon-13 INEPT in solid-state NMR spectroscopy. J Am Chem Soc 127:17296–17302CrossRefGoogle Scholar
  18. Fry SC (1989) The structure and functions of xyloglucan. J Exp Bot 40:1–11CrossRefGoogle Scholar
  19. Habibi Y, Heyraud A, Mahrouz M, Vignon MR (2004) Structural features of pectic polysaccharides from the skin of Opuntia ficus-indica prickly pear fruits. Carbohydr Res 339:1119–1127CrossRefGoogle Scholar
  20. Hardy EH, Verel R, Meier BH (2001) Fast MAS total through-bond correlation spectroscopy. J Magn Reson 148:459–464ADSCrossRefGoogle Scholar
  21. Harris DM et al (2012) Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1A903V and CESA3T942I of cellulose synthase. Proc Natl Acad Sci USA 109:4098–4103ADSCrossRefGoogle Scholar
  22. Hong M, Schmidt-Rohr K (2013) Magic-angle-spinning NMR techniques for measuring long-range distances in biological macromolecules. Acc Chem Res 46:2154–2163CrossRefGoogle Scholar
  23. Ishii T, Ichita J, Matsue H, Ono H, Maeda I (2002) Fluorescent labeling of pectic oligosaccharides with 2-aminobenzamide and enzyme assay for pectin. Carbohydr Res 337:1023–1032CrossRefGoogle Scholar
  24. Jarvis M (2003) Chemistry: cellulose stacks up. Nature 426:611–612ADSCrossRefGoogle Scholar
  25. Kirui A, Ling Z, Kang X, Dickwella Widanage MC, Mentink-Vigier F, French AD, Wang T (2019) Atomic resolution of cotton cellulose structure enabled by dynamic nuclear polarization solid-state NMR. Cellulose 26:329–339CrossRefGoogle Scholar
  26. Kobayashi H et al (1995) Assignment of 1H and 13C NMR chemical-shifts of α D-mannan composed of α-(1- > 2)-linkage and α-(1- > 6)-linkage obtained from Candida kefyr IFO 0586 strain. Carbohydr Res 267:299–306CrossRefGoogle Scholar
  27. Kobayashi H et al (1997) Structure of a cell wall mannan from the pathogenic yeast, Candida catenulata: assignment of 1H nuclear magnetic resonance chemical shifts of the inner α-1,6-linked mannose residues substituted by a side chain. Arch Biochem Biophys 341:70–74CrossRefGoogle Scholar
  28. Kumashiro KK, Schmidt-Rohr K, Murphy OJ, Ouellette KL, Cramer WA, Thompson LK (1998) A novel tool for probing membrane protein structure: solid-state NMR with proton spin diffusion and X-nucleus detection. J Am Chem Soc 120:5043–5051CrossRefGoogle Scholar
  29. Laguri C et al (2018) Solid state NMR studies of intact lipopolysaccharide endotoxin. ACS Chem Biol 13:2106–2113CrossRefGoogle Scholar
  30. Lange A, Luca S, Baldus M (2002) Structural constraints from proton-mediated rare-spin correlation spectroscopy in rotating solids. J Am Chem Soc 124:9704–9705CrossRefGoogle Scholar
  31. Lecoq L et al (2019) 100 kHz MAS proton-detected NMR spectroscopy of hepatitis B virus capsids. Front Mol Biosci 6:58CrossRefGoogle Scholar
  32. Lopez-Sanchez P, Martinez-Sanz M, Bonilla MR, Wang D, Gilbert EP, Stokes JR, Gidley MJ (2017) Cellulose-pectin composite hydrogels: intermolecular interactions and material properties depend on order of assembly. Carbohydr Polym 162:71–81CrossRefGoogle Scholar
  33. Lowman DW et al (2011) New insights into the structure of (1 - > 3,1 - > 6)-β-D-glucan side chains in the Candida glabrata cell wall. PLoS ONE 6:e27614ADSCrossRefGoogle Scholar
  34. Mandala VS, Hong M (2019) High-sensitivity protein solid-state NMR spectroscopy. Curr Opin Struct Biol.  https://doi.org/10.1016/j.sbi.2019.03.027 Google Scholar
  35. Mccann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. J Cell Sci 96:323–334Google Scholar
  36. 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. Can J Bot 73:S103–S113CrossRefGoogle Scholar
  37. Mortimer JC et al (2015) An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14. Plant J 83:413–426CrossRefGoogle Scholar
  38. Nars A et al (2013) Aphanomyces euteiches cell wall fractions containing novel glucan-chitosaccharides induce defense genes and nuclear calcium oscillations in the plant host Medicago truncatula. PLoS ONE 8:e75039ADSCrossRefGoogle Scholar
  39. Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Ib from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124:9074–9082CrossRefGoogle Scholar
  40. Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose Ia, from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125:14300–14306CrossRefGoogle Scholar
  41. Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol 56:180–194CrossRefGoogle Scholar
  42. Pena MJ, Kulkarni AR, Backe J, Boyd M, O’Neill MA, York WS (2016) Structural diversity of xylans in the cell walls of monocots. Planta 244:589–606CrossRefGoogle Scholar
  43. Phyo P, Wang T, Kiemle SN, O’Neill H, Pingali SV, Hong M, Cosgrove DJ (2017a) Gradients in wall mechanics and polysaccharides along growing inflorescence stems. Plant Physiol 175:1593–1607CrossRefGoogle Scholar
  44. Phyo P, Wang T, Xiao C, Anderson CT, Hong M (2017b) Effects of pectin molecular weight changes on the structure, dynamics, and polysaccharide interactions of primary cell walls of Arabidopsis thaliana: insights from solid-state NMR. Biomacromol 18:2937–2950CrossRefGoogle Scholar
  45. Phyo P, Gu Y, Hong M (2019) Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR. Cellulose 26:291–304CrossRefGoogle Scholar
  46. Schanda P et al (2014) Atomic model of a cell-wall cross-linking enzyme in complex with an intact bacterial peptidoglycan. J Am Chem Soc 136:17852–17860CrossRefGoogle Scholar
  47. Simmons TJ et al (2016) Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR. Nat Commun 7:13902ADSCrossRefGoogle Scholar
  48. Stanek J et al (2016) NMR spectroscopic assignment of backbone and side-chain protons in fully protonated proteins: microcrystals, sedimented assemblies, and amyloid fibrils. Angew Chem Int Ed Engl 55:15504–15509CrossRefGoogle Scholar
  49. Talbott LD, Ray PM (1992) Molecular-size and separability features of Pea cell wall polysaccharides. Implications for models of primary wall structure. Plant Physiol 98:357–368CrossRefGoogle Scholar
  50. Tan L, Varnai P, Lamport DT, Yuan C, Xu J, Qiu F, Kieliszewski MJ (2010) Plant O-hydroxyproline arabinogalactans are composed of repeating trigalactosyl subunits with short bifurcated side chains. J Biol Chem 285:24575–24583CrossRefGoogle Scholar
  51. Wang T, Hong M (2015) Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls. J Exp Bot 67:503–514CrossRefGoogle Scholar
  52. Wang T, Hong M (2016) Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls. J Exp Bot 67:503–514CrossRefGoogle Scholar
  53. Wang T, Zabotina O, Hong M (2012) Pectin-cellulose interactions in the Arabidopsis primary cell wall from two-dimensional magic-angle-spinning solid-state nuclear magnetic resonance. Biochemistry 51:9846–9856CrossRefGoogle Scholar
  54. 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. Proc Natl Acad Sci USA 110:16444–16449ADSCrossRefGoogle Scholar
  55. 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 53:2840–2854CrossRefGoogle Scholar
  56. Wang T, Park YB, Cosgrove DJ, Hong M (2015) Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis thaliana primary cell walls: evidence from solid-state NMR. Plant Physiol 168:871–883CrossRefGoogle Scholar
  57. Wang T, Phyo P, Hong M (2016a) Multidimensional solid-state NMR spectroscopy of plant cell walls. Solid State Nucl Magn Reson 78:56–63CrossRefGoogle Scholar
  58. Wang T, Yang H, Kubicki JD, Hong M (2016b) Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules 17:2210–2222CrossRefGoogle Scholar
  59. Wefers D, Tyl CE, Bunzel M (2014) Novel arabinan and galactan oligosaccharides from dicotyledonous plants. Front Chem 2:100CrossRefGoogle Scholar
  60. White PB, Wang T, Park YB, Cosgrove DJ, Hong M (2014) Water-polysaccharide interactions in the primary cell wall of Arabidopsis thaliana from polarization transfer solid-state NMR. J Am Chem Soc 136:10399–10409CrossRefGoogle Scholar
  61. Whitney SEC, Brigham JE, Darke AH, Reid JSG, Gidley MJ (1995) In-vitro assembly of cellulose/xyloglucan networks—ultrastructural and molecular aspects. Plant J 8:491–504CrossRefGoogle Scholar
  62. Wu X, Mort A (2014) Structure of a rhamnogalacturonan fragment from apple pectin: implications for pectin architecture. Int J Carbohydr Chem 2014:6CrossRefGoogle Scholar
  63. Yu B, van Ingen H, Vivekanandan S, Rademacher C, Norris SE, Freedberg DI (2012) More accurate 1 J(CH) coupling measurement in the presence of 3 J(HH) strong coupling in natural abundance. J Magn Reson 215:10–22ADSCrossRefGoogle Scholar
  64. Zhou DH, Rienstra CM (2008) High-performance solvent suppression for proton detected solid-state NMR. J Magn Reson 192:167–172ADSCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of ChemistryMassachusetts Institute of TechnologyCambridgeUSA

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