Skip to main content
Springer Nature Link
Log in

New cellulose synthesizing complexes (terminal complexes) involved in animal cellulose biosynthesis in the tunicateMetandrocarpa uedai

  • Published:
Protoplasma Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Summary

Cellulose synthesizing enzyme complexes (terminal complexes, TCs) have been found in the plasma membrane of epidermal cells in the tunicateMetandrocarpa uedai by using freeze-fracture replication techniques for electron microscopy. Assembly of cellulose microfibrils by TCs is a universal phenomenon in the biological kingdoms. The TCs are locally distributed in the plasma membrane of the epidermal cells facing the tunic, and no TCs are observed on the lateral membranes bordered by tight junctions. The TCs consist of two types of membrane subunits: large particles (14.5 nm in diameter) on the periphery and small subunit particles (7.2 nm) filling the center; the latter are hypothesized to be involved in cellulose synthesis. The TCs are the linear type (ca. 195 nm in length and 78 nm in width). Direct connections of TCs with the termini of microfibrils were observed. Amorphous regions, which were hypothesized the nascent microfibrils, were associated with the depressions of the TCs. The distortion of microfibrils on their terminus indicates that the crystallization may occur at the margin of TCs from which the microfibrils are discharged. This report provides evidence that: (1) The outer cell membrane of epidermis is the site for the assembly of cellulose microfibrils in the tunic; (2) a new type of TC is involved in the biosynthesis of cellulose microfibrils in the tunicates; (3) disorganized glucan chains may be synthesized in the depression of TCs and crystallized outside the E-surface of the epidermal cell membrane.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
€32.70 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Belton PS, Tanner SF, Cartier N, Chanzy H (1989) High-resolution solid-state13C nuclear magnetic resonance spectroscopy of tunicin, an animal cellulose. Macromolecules 22: 1615–1617

    Google Scholar 

  • Brown RM Jr (1985) Cellulose microfibril assembly and orientation: recent developments. J Cell Sci Suppl 2: 13–32

    PubMed  Google Scholar 

  • — (1990) Algae as tools in studying biosynthesis of cellulose, nature's most abundant macromolecule. In: Wiessner W, Robinson DG, Starr RC (eds) Cell walls and surfaces, reproduction, photosynthesis. Springer, Berlin Heidelberg New York Tokyo, pp 20–39

    Google Scholar 

  • —, Montezinos D (1976) Cellulose microfibril: visualization of biosynthetic and orienting complexes in association with the plasma membrane. Proc Natl Acad Sci USA 73: 143–147

    PubMed  Google Scholar 

  • —, Willison JH, Richardson CL (1976) Cellulose biosynthesis inAcetobacter xylinum: visualization of the site of synthesis and direct measurement of the in vivo process. Proc Natl Acad Sci USA 73: 4565–4569

    PubMed  Google Scholar 

  • Cloney RA, Cavey MJ (1982) Ascidian larval tunic: extraembryonic structures influence morphogenesis. Cell Tissue Res 222: 547–562

    PubMed  Google Scholar 

  • —, Grimm L (1970) Transcellular emigration of blood cells during ascidian metamorphosis. Z Zellforsch 107: 157–173

    PubMed  Google Scholar 

  • Deck JD, Hay ED, Revel J-P (1966) Fine structure and origin of the tunic ofPerophora viridis. J Morphol 120: 267–280

    PubMed  Google Scholar 

  • Dilly PN (1969) The ultrastructure of the tadpole larva ofCiona intestinalis. Z Zellforsch 95: 331–346

    PubMed  Google Scholar 

  • Emons AMC (1985) Plasma-membrane rosettes in root hair ofEquisetum hyemale. Planta 163: 350–359

    Google Scholar 

  • — (1991) Role of particle rosettes and terminal globules in cellulose synthesis. In: Haigler CH, Weimer PJ (eds) Biosynthesis and biodegradation of cellulose. Dekker, New York, pp 71–98

    Google Scholar 

  • Endean R (1955a) Studies of the blood and test of some Australian ascidians. II. The test ofPyura stolonifera (Heller). Aust J Mar Freshw Res 6: 139–156

    Google Scholar 

  • —, (1955b) Studies of the blood and test of some Australian ascidians. III. The formation of the test ofPyura stolonifera (Heller). Aust J Mar Freshw Res 6: 157–164

    Google Scholar 

  • —, (1961) The test of the ascidian,Phalusia mammillata. Q J Microsc Sci 102: 107–117

    Google Scholar 

  • Giddings TH Jr, Brower DL, Staehelin LA (1980) Visualization of particle complexes in the plasma membrane ofMicrasterias denticula associated with the formation of cellulose fibrils in primary and secondary cell walls. J Cell Biol 84: 327–339

    PubMed  Google Scholar 

  • Goodbody I (1974) The physiology of ascidian. Adv Mar Biol 12: 1–149

    Google Scholar 

  • Hotchkiss AT Jr, Brown RM Jr (1989) Evolution of the cellulosic cell wall in the Charophycea. In: Schuerch C (ed) Cellulose and wood: chemistry and technology. Wiley, New York, pp 591–609

    Google Scholar 

  • Itoh T (1990) Cellulose synthesizing complexes in some giant marine algae. J Cell Sci 95: 309–319

    Google Scholar 

  • —, Brown RM Jr (1984) The assembly of cellulose microfibrils inValonia macrophysa Kuts. Planta 160: 372–381

    Google Scholar 

  • Kalk M (1963) Intracellular sites of activity in the histogenesis of tunicate vanadocytes. Q J Microsc Sci 104: 483–493

    Google Scholar 

  • Katow H, Watanabe H (1978) Fine structure and possible role of ampullae on tunic supply and attachment in a compound ascidian,Botryllus primigenus OKA. J Ultrastruct Res 64: 23–34

    PubMed  Google Scholar 

  • Kimura S, Itoh T (1995) Evidence for the role of the glomerulocyte in cellulose synthesis in the tunicate,Metandrocarpa uedai. Protoplasma 186: 24–33

    Google Scholar 

  • Millar RH (1951) The stolonic vessels of the Didemnidae. Q J Microsc Sci 92: 249–254

    Google Scholar 

  • Mizuta S, Brown RM Jr (1992) High resolution analysis of the formation of cellulose synthesizing complexes inVaucheria hamata. Protoplasma 166: 187–199

    Google Scholar 

  • Mueller SC, Brown RM Jr (1980) Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. J Cell Biol 84: 315–326

    PubMed  Google Scholar 

  • Quader H (1991) Role of linear terminal complexes in cellulose synthesis. In: Haigler CH, Weimer PJ (eds) Biosynthesis and biodegradation of cellulose. M Dekker, New York, pp 51–69

    Google Scholar 

  • Rånby BG (1952) Physico-chemical investigations on animal cellulose (Tunicin). Arkiv Kemi 4: 241–248

    Google Scholar 

  • Revol J-F (1982) On the cross-sectional shape of cellulose crystallites inValonia ventricosa. Carbohydr Polymers 2: 123–134

    Google Scholar 

  • -Revol J-F, Van Daele Y, Gaill F (1990) On the cross-sectional shape of cellulose crystallites in the tunicateHalocynthia papillosa. In: Proceeding of the XIIth International Congress for Electron Microscopy, Seattle, August 12–18, 1996, pp 566–567

  • Robinson WE, Kustin K, Mcleod GC (1983) Incorporation of [14C]glucose into the tunic of the ascidian,Ciona intestinalis (Linnaeus). J Exp Zool 225: 187–195

    Google Scholar 

  • Seagull RW (1991) Role of the cytoskeletal elements in organized wall microfibril depositon. In: Haigler CH, Weimer PJ (eds) Biosynthesis and biodegradation of cellulose. M Dekker, New York, pp 143–163

    Google Scholar 

  • Smith MJ (1970) The blood cells and tunic of the ascidianHalocynthia aurantium (Pallas). I. Hematology, tunic morphology, and partitions of cells between blood and tunic. Biol Bull 138: 354–378

    Google Scholar 

  • Stiévenart J (1971) Recherches sur la morphologie et etude histchimique de la tunique d'Halocynthia papillosa Gun. (Ascidie Stlidobranche). Ann Soc R Zool Belg 101: 25–56

    Google Scholar 

  • Terakado K (1970) Tunic formation in the larva of an ascidian,Perophora orientalis. Sci Rep Saitama Univ 5B: 183–191

    Google Scholar 

  • Torrence SA, Cloney RA (1981) Rhythmic contraction of the ampullar epidermis during metamorphosis of the ascidianMolgura occidentalis. Cell Tissue Res 216: 293–312

    PubMed  Google Scholar 

  • Tsekos I, Reiss HD (1992) Occurrence of the putative microfibrilsynthesizing complexes (linear terminal complexes) in the plasma membrane of the epiphytic marine red algaeErytrocladia subintegra Rosenv. Protoplasma 169: 57–67

    Google Scholar 

  • Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32: 420–424

    PubMed  Google Scholar 

  • Van Daele Y, Revol J-F, Gaill F, Goffinet G (1992) Characterization and supermolecular architecture of the cellulose-protein fibrils in the tunic of the sea peach (Halocynthia papillosa, Ascidiaceae, Urochordata). Biol Cell 76: 87–96

    Google Scholar 

  • Wada M, Sugiyama J, Okano T (1995) Two crystalline phase (Iα/Iβ) system of native cellulose in relation to plant phylogenesis. Mokuzai Gakkaishi 41: 186–192

    Google Scholar 

  • Wardrop AB (1970) The structure and formation of test ofPyura stolonifera (Tunicata). Protoplasma 70: 73–86

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Wood Research Institute, Kyoto University, Uji, 611, Kyoto, Japan

    S. Kimura & T. Itoh

Authors
  1. S. Kimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kimura, S., Itoh, T. New cellulose synthesizing complexes (terminal complexes) involved in animal cellulose biosynthesis in the tunicateMetandrocarpa uedai . Protoplasma 194, 151–163 (1996). https://doi.org/10.1007/BF01882023

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01882023

Keywords

Search

Navigation