Journal of Wood Science

, Volume 55, Issue 6, pp 409–416 | Cite as

Nanostructural assembly of cellulose, hemicellulose, and lignin in the middle layer of secondary wall of ginkgo tracheid

  • Noritsugu Terashima
  • Kohei Kitano
  • Miho Kojima
  • Masato Yoshida
  • Hiroyuki Yamamoto
  • Ulla Westermark
Original Article


Physical, chemical, and biological properties of wood depend largely on the properties of cellulose, noncellulosic polysaccharides, and lignin, and their assembly mode in the cell wall. Information on the assembly mode in the main part of the ginkgo tracheid wall (middle layer of secondary wall, S2) was drawn from the combined results obtained by physical and chemical analyses of the mechanically isolated S2 and by observation under scanning electron microscopy. A schematic model was tentatively proposed as a basic assembly mode of cell wall polymers in the softwood tracheid as follows: a bundle of cellulose microfibrils (CMFs) consisting of about 430 cellulose chains is surrounded by bead-like tubular hemicellulose-lignin modules (HLM), which keep the CMF bundles equidistant from each other. The length of one tubular module along the CMF bundle is about 16 ± 2 nm, and the thickness at its side is about 3–4 nm. In S2, hemicelluloses are distributed in a longitudinal direction along the CMF bundle and in tangential and radial directions perpendicular to the CMF bundle so that they are aligned in the lamellae of tangential and radial directions with regard to the cell wall. One HLM contains about 7000 C6-C3 units of lignin, and 4000 hexose and 2000 pentose units of hemicellulose.

Key words

Cellulose microfibril Ginkgo biloba Hemicellulose Lignin Nanostructure 


  1. 1.
    Terashima N, Fukushima K, He LF, Takabe K (1993) Comprehensive model of the lignified plant cell wall. In: Jung HG, Buxton DR, Hatfield RD, Ralph J (eds) Forage cell wall structure and digestibility. American Society of Agronomy, Madison, USA, pp 247–270Google Scholar
  2. 2.
    Timell TE (1986) Origin and evolution of compression wood. In: Compression wood in gymnosperms. Springer, Berlin Heidelberg New York, pp 597–621CrossRefGoogle Scholar
  3. 3.
    Terashima N (2007) Non-destructive approaches to identify the ultrastructure of lignified ginkgo cell walls. Int J Plant Develop Biol 1:170–177Google Scholar
  4. 4.
    Terashima N, Akiyama T, Ralph S, Evtuguin D, Pascoal Neto C, Parkås J, Paulsson M, Westermark U, Ralph J (2009) 2D-NMR (HSQC) difference spectra between specifically 13C-enriched and unenriched protolignin of Ginkgo biloba obtained in the solution state of whole cell wall material. Holzforschung 63:379–384CrossRefGoogle Scholar
  5. 5.
    Terashima N, Yoshida M (2006) Observation of formation process of macromolecular lignin in the cell wall by electron microscope IV. Formation of hemicellulose-lignin module in black pine tracheid. Proceedings of the Annual Meeting of the Japan Wood Research Society Akita, Japan, PA005Google Scholar
  6. 6.
    Terashima N, Awano T, Takabe T, Yoshida M (2004) Formation of macromolecular lignin in ginkgo xylem cell walls as observed by field emission scanning electron microscopy. Comptes Rendus Biologies 327:903–910CrossRefPubMedGoogle Scholar
  7. 7.
    Terashima N, Yoshida M (2005) Ultrastructural assembly of polysaccharides and lignin in lignifying plant cell walls. Proceedings of 13th International Symposium on Wood, Fiber, and Pulping Chemistry, Auckland, New Zealand, vol 2, pp 423–426Google Scholar
  8. 8.
    Browning BL (1967) Preparation of holocellulose by chlorite methods (Wise method) and determination of alpha-cellulose content. In: Methods of wood chemistry, vol 2. Interscience, New York, p 395, 418Google Scholar
  9. 9.
    Dence CW (1992) Determination of lignin in wood and pulp by the acetyl bromide method. In: Lin SY, Dence CW (eds) Methods in lignin chemistry, Springer, Berlin Heidelberg New York, pp 44–48Google Scholar
  10. 10.
    Yamamoto H, Okuyama T, Yoshida M (1993) Method of determining the mean microfibril angle of wood over a wide range by the improved Cave’s method. Mokuzai Gakkaishi 39:375–381Google Scholar
  11. 11.
    Hafrén J, Fujino T, Itoh T (1999) Changes in cell wall architecture of differentiating tracheids of Pinus thunbergiii during lignification. Plant Cell Physiol 40:532–541CrossRefGoogle Scholar
  12. 12.
    Fahlén J, Salmén L (2003) Cross-sectional structure of the secondary wall of wood fibers as affected by processing. J Mater Sci 38:119–126CrossRefGoogle Scholar
  13. 13.
    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 124:9074–9082CrossRefPubMedGoogle Scholar
  14. 14.
    Kataoka Y, Kondo T (1996) Changing cellulose crystalline structure in forming wood cell walls. Macromolecules 29:6356–6358CrossRefGoogle Scholar
  15. 15.
    Herth W (1983) Arrays of plasma-membrane “grosettes” involved in cellulose microfibril formation of Spyrogyra. Planta 159:347–356CrossRefPubMedGoogle Scholar
  16. 16.
    Sugiyama J, Harada H, Fujiyoshi Y, Uyeda N (1985) Lattice images from ultrathin sections of cellulose microfibrils in the cell wall of Valonia macrophysa Kütz. Planta 166:161–168CrossRefPubMedGoogle Scholar
  17. 17.
    Helbert W, Nishiyama Y, Okano T, Sugiyama J (1998) Molecular imaging of Halocynthia papillosa cellulose. J Struct Biol 124:42–50CrossRefPubMedGoogle Scholar
  18. 18.
    Xu P, Donaldson LA, Gergely ZR, Staehelin A (2007) Dual axis electron tomography: a new approach for investigating the special organization of wood cellulose microfibrils. Wood Sci Technol 41:101–116CrossRefGoogle Scholar
  19. 19.
    Baker AA, Helbert W, Sugiyama J, Miles MJ (2000) New insight into cellulose structure by atomic force microscope shows the Iα crystal phase at near-atomic resolution. Biophys J 79:1139–1145CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Timell TE (1960) Studies on Ginkgo biloba L. 1. General characteristics and chemical composition. Sven Papperstidn 63:652–657Google Scholar
  21. 21.
    Mian J, Timell TE (1960) Studies on Ginkgo biloba L. 2. The constitution of an arabino-4-O-methyl-glucurono-xylan from the wood. Sven Papperstidn 63:769–774Google Scholar
  22. 22.
    Timell TE (1961) Isolation of galactoglucomannans from the wood of gymnosperms. TAPPI 44:88–96Google Scholar
  23. 23.
    Yoshida M, Hosoo Y, Okuyama T (2000) Periodicity as a factor in the generation of isotropic compressive growth stress between microfibrils in cell wall formation during a twenty-four hour period. Holzforschung 54:469–473Google Scholar
  24. 24.
    Hosoo Y, Imai T, Yoshida M (2006) Diurnal differences in the supply of glucomannanns and xylans in inner-most surface of cell walls at various developmental stages from cambium to mature xylem in Cryptomeria japonica. Protoplasma 229:11–19CrossRefPubMedGoogle Scholar
  25. 25.
    Tokoh C, Takabe K, Sugiyama J, Fujita M (2002) Cellulose synthesized by Acetobacter xylinum in the presence of plant cell wall polysaccharides. Cellulose 9:65–74CrossRefGoogle Scholar
  26. 26.
    Tokoh C, Takabe K, Sugiyama J, Fujita M (2002) CP/MAS 13C NMR and electron diffraction study of bacterial cellulose structure affected by cell wall polysaccharides. Cellulose 9:351–360CrossRefGoogle Scholar
  27. 27.
    Awano T, Takabe Y, Fujita M (2002) Xylan deposition on secondary wall of Fagus crenata fiber. Protoplasma 219:106–115CrossRefPubMedGoogle Scholar
  28. 28.
    Ralph J, Grabber JH, Hatfield RD (1995) Lignin-ferulate crosslink in grasses: active incorporation of ferulate polysaccharide esters into ryegrass lignins. Carbohydr Res 275:167–178CrossRefGoogle Scholar
  29. 29.
    Ralph J, Hatfield RD, Grabber JH, Jung H-JG, Quideau S, Helm RF (1998) Cell wall cross-linking in grasses by ferulates and diferulates. In: Lewis NG, Sarkanen S (eds) ACS Symposium Series 697, Lignin and lignan biosynthesis. American Chemical Society, Washington DC, pp 209–236Google Scholar
  30. 30.
    Ramiah MV, Goring DAI (1965) The thermal expansion of cellulose, hemicellulose, and lignin. J Polym Sci Part C 11:27–48CrossRefGoogle Scholar
  31. 31.
    Terashima N, Yoshida M (2006) Ultrastructure of lignified plant cell wall observed by field-emission scanning electron microscopy. Observations on periodate lignin prepared from Ginkgo biloba. Cellulose Chem Technol 40:727–733Google Scholar
  32. 32.
    Atalla RH, Agarwal UP (1986) Raman microprobe evidence for lignin orientation in the cell wall of native woody tissue. Science 227:636–638CrossRefGoogle Scholar
  33. 33.
    Agarwal UP, Atalla RH (1986) In-situ Raman microprobe studies of plant cell walls: macromolecular organization and compositional variability in the secondary wall of Picea mariana (Mill.) B.S.P. Planta 169:325–332CrossRefPubMedGoogle Scholar
  34. 34.
    Terashima N, Attala RH (1995) Formation and structure of plant cell wall - factors controlling lignin structure during its formation. Proceedings of the 8th International Symposium on Wood and Pulping Chemistry, Helsinki. Finland, vol 1, pp 69–76Google Scholar
  35. 35.
    Akiyama T, Ralph J (2008) Characteristics in 1H- and 13C-NMR chemical shifts of non-phenolic dibenzodioxocin model compounds as branch-points in lignin. Proceedings of 53rd Lignin Symposium, Tokyo, pp 84–87Google Scholar
  36. 36.
    Kukkola E, Koutaniemi S, Pollanen E, Gustafson M, Karuhnen P, Lundell TK, Saranpää P, Kilpäinen I, Teeri TH, Fagerstedt KV (2004) The dibenzodioxocin lignin substructure is abundant in the inner part of the secondary wall in Norway spruce and silver birch xylem. Planta 218:497–500CrossRefPubMedGoogle Scholar
  37. 37.
    Kukkola E, Saranpää P, Fagerstedt K (2008) Juvenile and compressed wood cell walls layers differ in lignin structure in Norway spruce and Scots pine. IAWA J 29:47–54CrossRefGoogle Scholar
  38. 38.
    Donaldson L (2007) Cellulose microfibril aggregates and their size variation with cell wall type. Wood Sci Technol 41:443–460CrossRefGoogle Scholar

Copyright information

© The Japan Wood Research Society 2009

Authors and Affiliations

  • Noritsugu Terashima
    • 1
  • Kohei Kitano
    • 2
  • Miho Kojima
    • 2
  • Masato Yoshida
    • 2
  • Hiroyuki Yamamoto
    • 2
  • Ulla Westermark
    • 1
  1. 1.STFI (Swedish Pulp and Paper Research Institute)StockholmSweden
  2. 2.Laboratory of Biomaterial Physics, Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan

Personalised recommendations