Cellular and Molecular Life Sciences

, Volume 68, Issue 9, pp 1623–1631 | Cite as

The crystalline phase of cellulose changes under developmental control in a marine chordate

  • Keisuke NakashimaEmail author
  • Atsuo Nishino
  • Yoshiki Horikawa
  • Euichi Hirose
  • Junji Sugiyama
  • Nori Satoh
Research Article


The native form of cellulose is a fibrillar composite of two crystalline phases, the triclinic Iα and monoclinic Iβ allomorphs. Allomorph ratios are species-specific, and this gives rise to natural structural variations in cellulose crystals. However, the mechanisms contributing to crystal formation remain unknown. We show that the two crystalline phases of cellulose are tailored to distinct structures during different developmental stages of the tunicate chordate Oikopleura dioica. Larval cellulose consisting of Iα allomorph constitutes the body cuticle fin, whereas adult cellulose consisting of Iβ allomorph frames a mucous filter-feeding device, the “house.” Both structures are secreted from the epidermis in accordance with the mutually exclusive expression patterns of two distinct putative cellulose synthase genes. We discuss a possible linkage between structural variations of the crystalline phases of cellulose and the underlying evolutionary genetics of cellulose biosynthesis.


Cellulose Allomorph Tunicate Appendicularian Oikopleura dioica 



We thank Dr. Tomoya Imai for valuable discussion, Dr. Yutaka Satou for the qPCR facility, Prof. Hiroyuki Yano for the FE-SEM facility, Dr. Fuki Gyoja for sampling Molgula tectiformis, and staff members of the Misaki Marine Biological Station, University of Tokyo, and Seto Marine Biological Station, Kyoto University, for sampling Oikopleura longicauda and Oikopleura dioica, respectively. The nucleotide sequences for the reported genes have been deposited with the GenBank under accession codes AB543594 (Od-CesA1) and AB543593 (Od-CesA2). K.N. designed research, performed experiments, and wrote the manuscript. A.N. performed collection, culture, and preparation of appendicularians. Y.H. and J.S. performed electron diffraction and FTIR microscopy. E.H. performed transmission electron microscopy. N.S. supervised reseach. All authors discussed the results and commented on the manuscript. The authors declare no competing financial interests. This work was supported by Grants-in-Aid for Young Scientists to K.N. (no. 18770046 and 21780166) and Grant-in-Aid to N.S. (no. 17018018) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan. This work was also partly supported by Intellectual Cluster Formation of Okinawa Prefecture, Japan.

Supplementary material

18_2010_556_MOESM1_ESM.doc (30 kb)
Supplementary material 1 (DOC 29 kb)
18_2010_556_MOESM2_ESM.pdf (221 kb)
Supplementary material 2 (PDF 221 kb)
18_2010_556_MOESM3_ESM.pdf (441 kb)
Supplementary material 3 (PDF 440 kb)

Supplementary material 4 (MP4 5947 kb)


  1. 1.
    Flood PR (1991) Architecture of, and water circulation and flow-rate in, the house of the planktonic tunicate Oikopleura labradoriensis. Mar Biol 111:95–111CrossRefGoogle Scholar
  2. 2.
    Gorsky G, Fenaux R (1998) The role of Appendicularia in marine food webs. In: Bone Q (ed) The biology of pelagic tunicates. Oxford University Press, New YorkGoogle Scholar
  3. 3.
    Sato R, Tanaka Y, Ishimaru T (2003) Species-specific house productivity of appendicularians. Mar Ecol Prog Ser 259:163–172CrossRefGoogle Scholar
  4. 4.
    Alldredge A (2005) The contribution of discarded appendicularian houses to the flux of particulate organic carbon from oceanic surface waters. In: Gorsky G, Youngbluth MJ, Deibel D (eds) Response of marine ecosystems to global change: ecological impact of Appendicularians. Editions Scientifiques GB, ParisGoogle Scholar
  5. 5.
    Nielsen C (2001) Animal evolution: interrelationships of the living phyla. Oxford University Press, New YorkGoogle Scholar
  6. 6.
    Fenaux R (1998) Life history of the appendicularia. In: Bone Q (ed) The biology of pelagic tunicates. Oxford University Press, New YorkGoogle Scholar
  7. 7.
    Kimura S, Ohshima C, Hirose E, Nishikawa J, Itoh T (2001) Cellulose in the house of the appendicularian Oikopleura rufescens. Protoplasma 216:71–74PubMedCrossRefGoogle Scholar
  8. 8.
    Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457:818–823PubMedCrossRefGoogle Scholar
  9. 9.
    Fujii S, Nishio T, Nishida H (2008) Cleavage pattern, gastrulation, and neurulation in the appendicularian, Oikopleura dioica. Dev Genes Evol 218:69–79PubMedCrossRefGoogle Scholar
  10. 10.
    Imai T, Sugiyama J (1998) Nanodomains of Iα and Iβ cellulose in algal microfibrils. Macromolecules 31:6275–6279CrossRefGoogle Scholar
  11. 11.
    Nakashima K, Sugiyama J, Satoh N (2008) A spectroscopic assessment of cellulose and the molecular mechanisms of cellulose biosynthesis in the ascidian Ciona intestinalis. Mar Genomics 1:9–14CrossRefGoogle Scholar
  12. 12.
    Imai T, Sugiyama J, Itoh T, Horii F (1999) Almost pure Iα cellulose in the cell wall of Glaucocystis. J Struct Biol 127:248–257PubMedCrossRefGoogle Scholar
  13. 13.
    Nishino A, Satou Y, Morisawa M, Satoh N (2001) Brachyury (T) gene expression and notochord development in Oikopleura longicauda (Appendicularia, Urochordata). Dev Genes Evol 211:219–231PubMedCrossRefGoogle Scholar
  14. 14.
    Nakashima K, Yamada L, Satou Y, Azuma J, Satoh N (2004) The evolutionary origin of animal cellulose synthase. Dev Genes Evol 214:81–88PubMedCrossRefGoogle Scholar
  15. 15.
    Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781PubMedCrossRefGoogle Scholar
  16. 16.
    Ganot P, Thompson EM (2002) Patterning through differential endoreduplication in epithelial organogenesis of the chordate, Oikopleura dioica. Dev Biol 252:59–71PubMedCrossRefGoogle Scholar
  17. 17.
    Flood PR (2005) Toward a photographic atlas on special taxonomic characters of oikopleurid Appendicularia (Tunicata). In: Gorsky G, Youngbluth MJ, Deibel D (eds) Response of marine ecosystems to global change: ecological impact of Appendicularians. Editions Scientifiques GB, ParisGoogle Scholar
  18. 18.
    Stach T (2007) Ontogeny of the appendicularian Oikopleura dioica (Tunicata, Chordata) reveals characters similar to ascidian larvae with sessile adults. Zoomorphology 126:203–214CrossRefGoogle Scholar
  19. 19.
    Goldstein MA, Takagi M, Hashida S, Shoseyov O, Doi RH, Segel IH (1993) Characterization of the cellulose-binding domain of the Clostridium cellulovorans cellulose-binding protein A. J Bacteriol 175:5762–5768PubMedGoogle Scholar
  20. 20.
    Belton PS, Tanner SF, Cartier N, Chanzy H (1989) High-resolution solid-state 13C nuclear magnetic resonance spectroscopy of tunicin, an animal cellulose. Macromolecules 22:1615–1617CrossRefGoogle Scholar
  21. 21.
    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 24:4168–4175CrossRefGoogle Scholar
  22. 22.
    Sugiyama J, Persson J, Chanzy H (1991) Combined infrared and electron diffraction study of the polymorphism of native celluloses. Macromolecules 24:2461–2466CrossRefGoogle Scholar
  23. 23.
    Marechal Y, Chanzy H (2000) The hydrogen bond network in Iβ cellulose as observed by infrared spectrometry. J Mol Struct 523:183–196CrossRefGoogle Scholar
  24. 24.
    Guerriero G, Fugelstad J, Bulone V (2010) What do we really know about cellulose biosynthesis in higher plants? J Integr Plant Biol 52:161–175PubMedCrossRefGoogle Scholar
  25. 25.
    Joshi CP, Mansfield SD (2007) The cellulose paradox-simple molecule, complex biosynthesis. Curr Opin Plant Biol 10:220–226PubMedCrossRefGoogle Scholar
  26. 26.
    Matthysse AG, Deschet K, Williams M, Marry M, White AR, Smith WC (2004) A functional cellulose synthase from ascidian epidermis. Proc Natl Acad Sci USA 101:986–991PubMedCrossRefGoogle Scholar
  27. 27.
    Mølhøj M, Pagant S, Höfte H (2002) Towards understanding the role of membrane-bound endo-beta-1,4-glucanases in cellulose biosynthesis. Plant Cell Physiol 43:1399–1406PubMedCrossRefGoogle Scholar
  28. 28.
    Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9:938–950PubMedCrossRefGoogle Scholar
  29. 29.
    Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, CambridgeGoogle Scholar
  30. 30.
    Nishiyama Y (2009) Structure and properties of the cellulose microfibril. J Wood Sci 55:241–249CrossRefGoogle Scholar
  31. 31.
    Cousins SK, Brown RM (1995) Cellulose I microfibril assembly: computational molecular mechanics energy analysis favours bonding by van der Waals forces as the initial step in crystallization. Polymer 36:3885–3888CrossRefGoogle Scholar
  32. 32.
    Cousins SK, Brown RM (1997) X-ray diffraction and ultrastructural analyses of dye-altered celluloses support van der Waals forces as the initial step in cellulose crystallization. Polymer 38:896–902Google Scholar
  33. 33.
    Cousins SK, Brown RM (1997) Photoisomerization of a dye-altered β-1,4 glucan sheet induces the crystallization of a cellulose-composite. Polymer 38:903–912CrossRefGoogle Scholar
  34. 34.
    Elbaum R, Zaltzman L, Burgert I, Fratzl P (2007) The role of wheat awns in the seed dispersal unit. Science 316:884–886PubMedCrossRefGoogle Scholar
  35. 35.
    Nobles DR, Brown RM (2007) Many paths up the mountain: tracking the evolution of cellulose biosynthesis. In: Brown RM, Saxena IM (eds) Cellulose: molecular and structural biology. Springer, DordrechtGoogle Scholar
  36. 36.
    Pasini A, Amiel A, Rothbacher U, Roure A, Lemaire P, Darras S (2006) Formation of the ascidian epidermal sensory neurons: insights into the origin of the chordate peripheral nervous system. PLoS Biol 4:1173–1186CrossRefGoogle Scholar
  37. 37.
    Kimura S, Itoh T (2007) Biogenesis and function of cellulose in tunicates. In: Brown RM, Saxena IM (eds) Cellulose: molecular and structural biology. Springer, DordrechtGoogle Scholar
  38. 38.
    Hirose E (2009) Ascidian tunic cells: morphology and functional diversity of free cells outside the epidermis. Invertebr Biol 128:83–96CrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2010

Authors and Affiliations

  • Keisuke Nakashima
    • 1
    • 2
    Email author
  • Atsuo Nishino
    • 3
  • Yoshiki Horikawa
    • 4
  • Euichi Hirose
    • 5
  • Junji Sugiyama
    • 4
  • Nori Satoh
    • 1
  1. 1.Marine Genomics UnitOkinawa Institute of Science and Technology Promotion CorporationOkinawaJapan
  2. 2.Department of Zoology, Graduate School of ScienceKyoto UniversityKyotoJapan
  3. 3.Department of Biological Sciences, Graduate School of ScienceOsaka UniversityToyonakaJapan
  4. 4.Research Institute for Sustainable HumanosphereKyoto UniversityUjiJapan
  5. 5.Department of Chemistry, Biology and Marine Science, Faculty of ScienceUniversity of the RyukyusOkinawaJapan

Personalised recommendations