, Volume 25, Issue 7, pp 3755–3777 | Cite as

An evaluation of the structures of cellulose generated by the CHARMM force field: comparisons to in planta cellulose

  • Daniel P. Oehme
  • Hui Yang
  • James D. Kubicki
Original Paper


Molecular dynamics simulations of cellulose regularly sample a conformational space different to the crystal structures they were initiated from, with changes to the tilt of chains, expansion of the unit cell and variation in exocyclic group conformations. Given the differences in the structures sampled the question presents itself as to whether these simulations are sampling structures that resemble cellulose in planta. To investigate this question, we have performed MD simulations on different size and shaped Iα and Iβ cellulose microfibrils with the structures generated characterized with regards to changes in expansion, chain shift along the polymerization axis, tilt, exocyclic conformation and H-bonding. Structures were then input into a quantum mechanical NMR chemical shift calculation protocol with the resulting 13C chemical shifts compared to experimental data. Chemical shifts were shown to be strongly dependent on the exocyclic group conformation with the structures of Iα simulations more closely replicating experimental data than the Iβ simulations, especially at the C4 and C6 positions which suggests that the conformational space was not being accurately represented for the Iβ microfibrils. Despite this, peak sizes based on the sampling occupancy of exocyclic conformations from unrestrained simulations were found to replicate experimental peak sizes better than simulations where exocyclic groups of interior chains were restrained to the tg conformation, suggesting that exocyclic groups have greater freedom to sample different conformations than suggested by their crystal structures.


Cellulose Microfibril Molecular dynamics NMR Quantum mechanics Exocyclic group 



This work was partly funded by a grant from the Australia Research Council (ARC) to the ARC Centre of Excellence in Plant Cell Walls (DPO) [CE110001007]; the Victorian Life Sciences Computation Initiative (VLSCI) grant number “VR0319” on its Peak Computing Facility at the University of Melbourne, an initiative of the Victorian State Government; and 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. Parts of this work were completed while DPO was at IBM Research—Australia. Portions of this research were conducted with Advanced Cyber Infrastructure computational resources provided by the Institute for Cyber Science at The Pennsylvania State University ( We also thank Prof. Mei Hong for the experimental triple mutant intact Arabidopsis spectra.

Supplementary material

10570_2018_1793_MOESM1_ESM.docx (716 kb)
Supplementary material 1 (DOCX 716 kb)


  1. Adamo C, Barone V (1998) Exchange functionals with improved long-range behavior and adiabatic connection methods without adjustable parameters: the mPW and mPW1PW models. J Chem Phys 108:664–675. CrossRefGoogle Scholar
  2. Alekozai EM, GhattyVenkataKrishna PK, Uberbacher EC et al (2014) Simulation analysis of the cellulase Cel7A carbohydrate binding module on the surface of the cellulose Iβ. Cellulose 21:951–971. CrossRefGoogle Scholar
  3. Angles Dortoli T, Sjöberg NA, Vasiljeva P et al (2015) Temperature Dependence of Hydroxymethyl Group Rotamer Populations in Cellooligomers. J Phys Chem B 119:9559–9570. CrossRefGoogle Scholar
  4. Atalla RH, Van der Hart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 80(23):283–285CrossRefGoogle Scholar
  5. Barnett CB, Naidoo KJ (2008) Stereoelectronic and solvation effects determine hydroxymethyl conformational preferences in monosaccharides. J Phys Chem B 112:15450–15459. CrossRefPubMedGoogle Scholar
  6. Beckham GT, Matthews JF, Peters B et al (2011) Molecular-level origins of biomass recalcitrance: decrystallization free energies for four common cellulose polymorphs. J Phys Chem B 115:4118–4127. CrossRefPubMedGoogle Scholar
  7. Bergenstråhle M, Thormann E, Nordgren N, Berglund LA (2009) Force pulling of single cellulose chains at the crystalline cellulose-liquid interface: a molecular dynamics study. Langmuir 25:4635–4642. CrossRefPubMedGoogle Scholar
  8. Brett CT (2000) Cellulose microfibrils in plants: biosynthesis, deposition, and integration into the cell wall. Int Rev Cytol 199:161–199. CrossRefPubMedGoogle Scholar
  9. Bu L, Himmel ME, Crowley MF (2015) The molecular origins of twist in cellulose I-beta. Carbohydr Polym 125:146–152. CrossRefPubMedGoogle Scholar
  10. Bučko T, Tunega D, Ángyán JG, Hafner J (2011) Ab initio study of structure and interconversion of native cellulose phases. J Phys Chem A 115:10097–10105. CrossRefPubMedGoogle Scholar
  11. Bühl M, Kaupp M, Malkina OL, Malkin VG (1999) The DFT route to NMR chemical shifts. J Comput Chem 20:91–105.<91::aid-jcc10>;2-cGoogle Scholar
  12. Busse-Wicher M, Gomes TCF, Tryfona T et al (2014) The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a two-fold helical screw in the secondary plant cell wall of Arabidopsis thaliana. Plant J 79:492–506. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cheeseman JR, Trucks GW, Keith TA, Frisch MJ (1996) A comparison of models for calculating nuclear magnetic resonance shielding tensors. J Chem Phys 104:5497–5509. CrossRefGoogle Scholar
  14. Chen P, Nishiyama Y, Putaux J-L, Mazeau K (2014) Diversity of potential hydrogen bonds in cellulose I revealed by molecular dynamics simulation. Cellulose 21:897–908. CrossRefGoogle Scholar
  15. Ciesielski PN, Matthews JF, Tucker MP et al (2013) 3D electron tomography of pretreated biomass informs atomic modeling of cellulose microfibrils. ACS Nano 7:8011–8019. CrossRefPubMedGoogle Scholar
  16. Conley K, Godbout L, Whitehead MA, Van De Ven TGM (2016) Origin of the twist of cellulosic materials. Carbohydr Polym 135:285–299. CrossRefPubMedGoogle Scholar
  17. Devarajan A, Markutsya S, Lamm MH et al (2013) Ab initio study of molecular interactions in cellulose Iα. J Phys Chem B 117:10430–10443. CrossRefPubMedGoogle Scholar
  18. Djahedi C, Berglund LA, Wohlert J (2015) Molecular deformation mechanisms in cellulose allomorphs and the role of hydrogen bonds. Carbohydr Polym 130:175–182. CrossRefPubMedGoogle Scholar
  19. Elazzouzi-Hafraoui S, Nishiyama Y, Putaux JL et al (2008) The shape and size distribution of crystalline nanoparticles prepared by acid hydrolysis of native cellulose. Biomacromol 9:57–65. CrossRefGoogle Scholar
  20. Fernandes AN, Thomas LH, Altaner CM et al (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci USA 108:E1195–E1203. CrossRefPubMedGoogle Scholar
  21. Funahashi R, Okita Y, Hondo H, et al (2017) Different conformations of surface cellulose molecules in native cellulose microfibrils revealed by layer-by-layer peeling. 0–3.
  22. Gomes TCF, Skaf MS (2012) Cellulose-builder: a toolkit for building crystalline structures of cellulose. J Comput Chem 33:1338–1346. CrossRefPubMedGoogle Scholar
  23. Gottlieb HE, Kotlyar V, Nudelman A (1997) NMR chemical shifts of common laboratory solvents as trace impurities. J Org Chem 62:7512–7515. CrossRefPubMedGoogle Scholar
  24. Gross AS, Chu J-W (2010) On the molecular origins of biomass recalcitrance: the interaction network and solvation structures of cellulose microfibrils. J Phys Chem B 114:13333–13341. CrossRefPubMedGoogle Scholar
  25. Gross AS, Bell AT, Chu J-W (2011) Thermodynamics of cellulose solvation in water and the ionic liquid 1-butyl-3-methylimidazolim chloride. J Phys Chem B 115:13433–13440. CrossRefPubMedGoogle Scholar
  26. Guvench O, Greene SN, Kamath G et al (2008) Additive empirical force field for hexopyranose monosaccharides. J Comput Chem 29:2543–2564. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Guvench O, Mallajosyula SS, Raman EP et al (2011) CHARMM additive all-atom force field for carbohydrate derivatives and its utility in polysaccharide and carbohydrate-protein modeling. J Chem Theory Comput 7:3162–3180. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hadden JA, French AD, Woods RJ (2013) Unraveling cellulose microfibrils: a twisted tale. Biopolymers 99:746–756. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hadden JA, French AD, Woods RJ (2014) Effect of microfibril twisting on theoretical powder diffraction patterns of cellulose I? Cellulose 21:879–884. CrossRefPubMedGoogle Scholar
  30. Hanley S, Revol J-F, Godbout L, Gray D (1997) Atomic force microscopy and transmission electron microscopy of cellulose from Micrasterias denticulata; evidence for a chiral helical microfibril twist. Cellulose 4:209–220. CrossRefGoogle Scholar
  31. Hansen HS, Hünenberger PH (2011) A reoptimized GROMOS force field for hexopyranose-based carbohydrates accounting for the relative free energies of ring conformers, anomers, epimers, hydroxymethyl rotamers, and glycosidic linkage conformers. J Comput Chem 32:998–1032. CrossRefPubMedGoogle Scholar
  32. Hanus J, Mazeau K (2006) The xyloglucan—cellulose assembly at the atomic scale. Biopolymers 82:59–73. CrossRefPubMedGoogle Scholar
  33. Heiner AP, Kuutti L, Teleman O (1998) Comparison of the interface between water and four surfaces of native crystalline cellulose by molecular dynamics simulations. Carbohydr Res 306:205–220. CrossRefGoogle Scholar
  34. Hill JL, Hammudi MB, Tien M (2014) The arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. Plant Cell Online 26:4834–4842. CrossRefGoogle Scholar
  35. Horii F, Hirai A, Kitamaru R (1983) Solid-state 13C-NMR study of conformations of oligosaccharides and cellulose conformation of CH2OH group about the exo-cyclic C–C bond. Polym Bull 10:357–361CrossRefGoogle Scholar
  36. Kafle K, Lee CM, Shin H et al (2015) Effects of delignification on crystalline cellulose in lignocellulose biomass characterized by vibrational sum frequency generation spectroscopy and X-ray diffraction. Bioenergy Res 8:1750–1758. CrossRefGoogle Scholar
  37. Kannam SK, Oehme DP, Doblin MS et al (2017) Hydrogen bonds and twist in cellulose microfibrils. Carbohydr Polym 175:433–439. CrossRefPubMedGoogle Scholar
  38. Karadakov PB (2006) Ab initio calculation of NMR shielding constants. Modern magnetic resonance. Springer, Dordrecht, pp 63–70CrossRefGoogle Scholar
  39. Kim SH, Lee CM, Kafle K (2013) Characterization of crystalline cellulose in biomass: basic principles, applications, and limitations of XRD, NMR, IR, Raman, and SFG. Korean J Chem Eng 30:2127–2141. CrossRefGoogle Scholar
  40. Kirschner KN, Yongye AB, Tschampel SM et al (2007) GLYCAM06: a generalizable biomolecular force field. Carbohydrates. J Comput Chem 29:622–655. CrossRefGoogle Scholar
  41. Kono H, Numata Y (2006) Structural investigation of cellulose Iα and Iβ by 2D RFDR NMR spectroscopy: determination of sequence of magnetically inequivalent d-glucose units along cellulose chain. Cellulose 13:317–326. CrossRefGoogle Scholar
  42. Kubicki JD, Mohamed MN-A, Watts HD (2013) Quantum mechanical modeling of the structures, energetics and spectral properties of Iα and Iβ cellulose. Cellulose 20:9–23. CrossRefGoogle Scholar
  43. Kubicki JD, Watts HD, Zhao Z, Zhong L (2014) Quantum mechanical calculations on cellulose–water interactions: structures, energetics, vibrational frequencies and NMR chemical shifts for surfaces of Iα and Iβ cellulose. Cellulose 21:909–926. CrossRefGoogle Scholar
  44. Kuttel M, Brady JW, Naidoo KJ (2002) Carbohydrate solution simulations: producing a force field with experimentally consistent primary alcohol rotational frequencies and populations. J Comput Chem 23:1236–1243. CrossRefPubMedGoogle Scholar
  45. Langan P, Petridis L, O’Neill HM et al (2014) Common processes drive the thermochemical pretreatment of lignocellulosic biomass. Green Chem 16:63. CrossRefGoogle Scholar
  46. Larsson PT, Westlund P-O (2005) Line shapes in CP/MAS (13)C NMR spectra of cellulose I. Spectrochim Acta A Mol Biomol Spectrosc 62:539–546. CrossRefPubMedGoogle Scholar
  47. Larsson PT, Wickholm K, Iversen T (1997) A CP/MAS 13C NMR investigation of molecular ordering in celluloses. Carbohydr Res 302:19–25CrossRefGoogle Scholar
  48. Lee CM, Kafle K, Park YB, Kim SH (2014) Probing crystal structure and mesoscale assembly of cellulose microfibrils in plant cell walls, tunicate tests, and bacterial films using vibrational Sum Frequency Generation (SFG) spectroscopy. Phys Chem Chem Phys 16:10844–10853. CrossRefPubMedGoogle Scholar
  49. Lee CM, Kubicki JD, Fan B, et al (2015) Hydrogen-bonding network and OH stretch vibration of cellulose: comparison of computational modeling with polarized IR and SFG spectra. J Phys Chem B.
  50. Li Y, Lin M, Davenport JW (2011) Ab initio studies of cellulose I: crystal structure, intermolecular forces, and interactions with water. J Phys Chem C 115:11533–11539. CrossRefGoogle Scholar
  51. Lindner B, Petridis L, Schulz R, Smith JC (2013) Solvent-driven preferential association of lignin with regions of crystalline cellulose in molecular dynamics simulation. Biomacromol 14:3390–3398. CrossRefGoogle Scholar
  52. Lodewyk MW, Siebert MR, Tantillo DJ (2012) Computational prediction of 1H and 13C chemical shifts: a useful tool for natural product, mechanistic, and synthetic organic chemistry. Chem Rev 112:1839–1862. CrossRefPubMedGoogle Scholar
  53. Matthews JF, Bergenstråhle M, Beckham GT et al (2011a) High-temperature behavior of cellulose I. J Phys Chem B 115:2155–2166. CrossRefPubMedGoogle Scholar
  54. Matthews JF, Himmel ME, Crowley MF (2011b) Conversion of cellulose Iα to Iβ via a high temperature intermediate (I-HT) and other cellulose phase transformations. Cellulose 19:297–306. CrossRefGoogle Scholar
  55. Matthews JF, Beckham GT, Bergenstråhle-Wohlert M et al (2012) Comparison of cellulose Iβ simulations with three carbohydrate force fields. J Chem Theory Comput 8:735–748. CrossRefPubMedGoogle Scholar
  56. Maurer RJ, Sax AF, Ribitsch V (2013) Moleular simulation of surface reorganization and wetting in crystalline cellulose I and II. Cellulose 20:25–42. CrossRefGoogle Scholar
  57. Mazeau K, Vergelati C (2002) Atomistic modeling of the adsorption of benzophenone onto cellulosic surfaces. Langmuir 18:1919–1927. CrossRefGoogle Scholar
  58. Miyamoto H, Schnupf U, Brady JW (2014) Water structuring over the hydrophobic surface of cellulose. J Agric Food Chem 62:11017–11023. CrossRefPubMedGoogle Scholar
  59. Moon RJ, Martini A, Nairn J et al (2011) Cellulose nanomaterials review: structure, properties and nanocomposites. Chem Soc Rev 40:3941. CrossRefPubMedGoogle Scholar
  60. Nawrocki G, Cazade PA, Thompson D, Cieplak M (2015) Peptide recognition capabilities of cellulose in molecular dynamics simulations. J Phys Chem C 119:24404–24416. CrossRefGoogle Scholar
  61. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  62. 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 Physiol 163:1558–1567. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Iβ from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124:9074–9082. CrossRefPubMedGoogle Scholar
  64. Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose Iα from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125:14300–14306. CrossRefPubMedGoogle Scholar
  65. Nishiyama Y, Johnson GP, French AD (2012) Diffraction from nonperiodic models of cellulose crystals. Cellulose 19:319–336. CrossRefGoogle Scholar
  66. Nishiyama Y, Langan P, O’Neill H et al (2014) Structural coarsening of aspen wood by hydrothermal pretreatment monitored by small- and wide-angle scattering of X-rays and neutrons on oriented specimens. Cellulose 21:1015–1024. CrossRefGoogle Scholar
  67. Nixon BT, Mansouri K, Singh A et al (2016) Comparative structural and computational analysis supports eighteen cellulose synthases in the plant cellulose synthesis complex. Sci Rep 6:28696. CrossRefPubMedPubMedCentralGoogle Scholar
  68. O’Neill H, Pingali SV, Petridis L et al (2017) Dynamics of water bound to crystalline cellulose. Sci Rep 7:11840. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Oehme DP, Doblin MS, Wagner J et al (2015a) Gaining insight into cell wall cellulose macrofibril organisation by simulating microfibril adsorption. Cellulose 22:3501–3520. CrossRefGoogle Scholar
  70. Oehme DP, Downton MT, Doblin MS et al (2015b) Unique aspects of the structure and dynamics of Iβ elementary cellulose microfibrils revealed by computational simulations. Plant Physiol 168:3–17. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Paavilainen S, Rog T, Vattulainen I (2011) Analysis of twisting of cellulose nanofibrils in atomistic molecular dynamics simulations. J Phys Chem B 115:3747–3755. CrossRefPubMedGoogle Scholar
  72. Park YB, Lee CM, Koo B-W et al (2013) Monitoring meso-scale ordering of cellulose in intact plant cell walls using sum frequency generation spectroscopy. Plant Physiol 163:907–913. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Payne CM, Himmel ME, Crowley MF, Beckham GT (2011) Decrystallization of oligosaccharides from the cellulose Iβ surface with molecular simulation. J Phys Chem Lett 2:1546–1550. CrossRefGoogle Scholar
  74. Pereira CS, Silveira RL, Dupree P, Skaf MS (2017) Effects of xylan side-chain substitutions on xylan-cellulose interactions and implications for thermal pretreatment of cellulosic biomass. Biomacromol 18:1311–1321. CrossRefGoogle Scholar
  75. Peri S, Muthukumar L, Nazmul Karim M, Khare R (2012) Dynamics of cello-oligosaccharides on a cellulose crystal surface. Cellulose 19:1791–1806. CrossRefGoogle Scholar
  76. Petridis L, O’Neill HM, Johnsen M et al (2014) Hydration control of the mechanical and dynamical properties of cellulose. Biomacromol 15:4152–4159. CrossRefGoogle Scholar
  77. Phillips JC, Braun R, Wang W et al (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781–1802. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Rassolov VA, Ratner MA, Pople JA et al (2001) 6-31G* basis set for third-row atoms. J Comput Chem 22:976–984. CrossRefGoogle Scholar
  79. Rockwell GD, Grindley TB (1998) Effect of solvation on the rotation of hydroxymethyl groups in carbohydrates. J Am Chem Soc 120:10953–10963. CrossRefGoogle Scholar
  80. Sarotti AM, Pellegrinet SC (2009) A multi-standard approach for GIAO 13C NMR calculations. J Org Chem 74:7254–7260. CrossRefPubMedGoogle Scholar
  81. Schreckenbach G, Ziegler T (1995) Calculation of NMR shielding tensors using gauge-including atomic orbitals and modern density functional theory. J Phys Chem 99:606–611. CrossRefGoogle Scholar
  82. Shklyaev OE, Kubicki JD, Watts HD, Crespi VH (2014) Constraints on Iβ cellulose twist from DFT calculations of 13C NMR chemical shifts. Cellulose 21:3979–3991. CrossRefGoogle Scholar
  83. Silveira RL, Stoyanov SR, Kovalenko A, Skaf MS (2016) Cellulose aggregation under hydrothermal pretreatment conditions. Biomacromol. CrossRefGoogle Scholar
  84. Srinivas G, Cheng X, Smith JC (2014) Coarse-grain model for natural cellulose fibrils in explicit water. J Phys Chem B 118:3026–3034. CrossRefPubMedGoogle Scholar
  85. Stenutz R, Carmichael I, Widmalm G, Serianni AS (2002) Hydroxymethyl group conformation in saccharides: structural dependencies of 2 J HH, 3 J HH, and 1 J CH spin–spin coupling constants. J Org Chem 67:949–958. CrossRefPubMedGoogle Scholar
  86. Sugiyama J, Vuong R, Chanzy H (1991) Electron diffraction study on the two crystalline phases occurring in native cellulose from an algal cell wall. Macromolecules 24:4168–4175. CrossRefGoogle Scholar
  87. Thibaudeau C, Stenutz R, Hertz B et al (2004) Correlated C–C and C–O bond conformations in saccharide hydroxymethyl groups: parametrization and application of redundant 1 H–1 H, 13 C–1 H, and 13 C–13 C NMR J-couplings. J Am Chem Soc 126:15668–15685. CrossRefPubMedGoogle Scholar
  88. Thomas LH, Forsyth VT, Sturcová A et al (2013) Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiol 161:465–476. CrossRefPubMedGoogle Scholar
  89. Thomas LH, Forsyth VT, Martel A et al (2015) Diffraction evidence for the structure of cellulose microfibrils in bamboo, a model for grass and cereal celluloses. BMC Plant Biol 15:153. CrossRefPubMedPubMedCentralGoogle Scholar
  90. Vandavasi VG, Putnam DK, Zhang Q et al (2016) A structural study of CESA1 catalytic domain of arabidopsis cellulose synthesis complex: evidence for CESA trimers. Plant Physiol 170:123–135. CrossRefPubMedGoogle Scholar
  91. Van der Hart DL, Atalla RH (1984) Studies of microstructure in native celluloses using solid-state 13C NMR. Macromolecules 17:1465–1472CrossRefGoogle Scholar
  92. Viëtor RJ, Newman RH, Ha M-A et al (2002) Conformational features of crystal-surface cellulose from higher plants. Plant J 30:721–731CrossRefGoogle Scholar
  93. 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 67:503–514. CrossRefPubMedGoogle Scholar
  94. 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 51:9846–9856. CrossRefPubMedGoogle Scholar
  95. Wang T, Yang H, Kubicki JD, Hong M (2016) Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules.
  96. Watts HD, Mohamed MNA, Kubicki JD (2011) 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 115:1958–1970. CrossRefPubMedGoogle Scholar
  97. Watts HD, Mohamed MNA, Kubicki JD (2014) A DFT study of vibrational frequencies and 13C NMR chemical shifts of model cellulosic fragments as a function of size. Cellulose 21:53–70. CrossRefGoogle Scholar
  98. Wiitala KW, Hoye TR, Cramer CJ (2006) Hybrid density functional methods empirically optimized for the computation of 13C and 1H chemical shifts in chloroform solution. J Chem Theory Comput 2:1085–1092. CrossRefPubMedGoogle Scholar
  99. Wolinski K, Hinton JF, Pulay P (1990) Efficient implementation of the gauge-independent atomic orbital method for NMR chemical shift calculations. J Am Chem Soc 112:8251–8260. CrossRefGoogle Scholar
  100. Yamamoto H, Horii F, Odani H (1989) Structural changes of native cellulose crystals induced by annealing in aqueous alkaline and acidic solutions at high temperatures. Macromolecules 22:4130–4132. CrossRefGoogle Scholar
  101. Yang H, Wang T, Oehme D et al (2018) Structural factors affecting 13C NMR chemical shifts of cellulose: a computational study. Cellulose 25:23–36. CrossRefGoogle Scholar
  102. Zhang T, Zheng Y, Cosgrove DJ (2016) Spatial organization of cellulose microfibrils and matrix polysaccharides in primary plant cell walls as imaged by multichannel atomic force microscopy. Plant J 85:179–192. CrossRefPubMedGoogle Scholar
  103. Zhao G, Perilla JR, Yufenyuy EL et al (2013a) Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497:643–646. CrossRefPubMedPubMedCentralGoogle Scholar
  104. Zhao Z, Shklyaev OE, Nili A et al (2013b) Cellulose microfibril twist, mechanics, and implication for cellulose biosynthesis. J Phys Chem A 117:2580–2589. CrossRefPubMedGoogle Scholar
  105. Zhao Z, Crespi VH, Kubicki JD et al (2014) Molecular dynamics simulation study of xyloglucan adsorption on cellulose surfaces: effects of surface hydrophobicity and side-chain variation. Cellulose 21:1025–1039. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Daniel P. Oehme
    • 1
    • 2
  • Hui Yang
    • 3
  • James D. Kubicki
    • 1
  1. 1.Department of Geological SciencesUniversity of Texas at El PasoEl PasoUSA
  2. 2.ARC Centre of Excellence in Plant Cell Walls, School of BioSciencesThe University of MelbourneParkvilleAustralia
  3. 3.Department of BiologyPennsylvania State UniversityUniversity ParkUSA

Personalised recommendations