Skip to main content
SpringerLink
Log in

Helicoidal orientation of cellulose microfibrils in Nitella opaca internode cells: ultrastructure and computed theoretical effects of strain reorientation during wall growth

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The ultrastructure of the mature internode cell wall of Nitella opaca is described. It is interpreted in terms of a helicoidal array of cellulose microfibrils set in a matrix. A helicoid is a multiple ‘plywood’ made up of layers of parallel microfibrils. There is a progressive change in direction from ply to ply, giving rise to characteristic arced patterns in oblique sections. A critical tilting test, using an electron microscope fitted with a goniometric stage, showed the expected reversal of direction of the arced pattern. Nitella cell wall is thus more regularly structured than previous studies have shown. From a survey of the cell-wall literature, we show that such arced patterns are common. This indicates that the helicoidal structure may be more widespread than is generally realised, although numerous other cell walls show no signs of it. Nevertheless, there are examples in most major plant taxa, and in several types of cells, including wood tracheids. Most of the examples, however, need confirmation by tilting evidence. There are possible implications for wall morphogenesis. Helicoidal cell walls might arise by selfassembly via a liquid crystalline phase, since it is known that the cholesteric state is itself helicoidal. A computer graphics programme has been developed to plot the expected effects of growth strain on the patterns in oblique sections of helicoids with various original angles between consecutive layers. Herringbone patterns typical of crossed polylamellate texture can be generated in this way, indicating a possible mode of their formation.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Appelbaum, A., Burg, S.P. (1971) Altered cell microfibrillar orientation in ethylene-treated Pisum sativum stems. Plant Physiol. 48, 648–652

    Google Scholar 

  • Barnabus, A.D., Butler, V., Steinke, T.D. (1977) Zostera capensis Setchell. I. Observations on the fine structure of the leaf epidermis. Z. Pflanzenphysiol. 85, 417–427

    Google Scholar 

  • Baynes, S.M. (1972) Light and electron microscope studies on the germination of Chara oospores. B.Sc. thesis project, Bristol University

  • Benedict, C.R., Scott, J.R. (1976) Photosynthetic carbon metabolism of a marine grass. Plant Physiol. 57, 876–880

    Google Scholar 

  • Birch, W.R. (1974) The unusual epidermis of the marine angiosperm Halophila Thou. Flora (Jena) 163, 410–414

    Google Scholar 

  • Bonfante-Fasolo, P. (1983) Electron microscopic cytochemical study of cell wall in Glomus epigaeum spore. (Abstr.) Third Int. Mycol. Congr., Tokyo, p. 392

  • Bonfante-Fasolo, P., Vian, B. (1984) Wall texture in the spore of a vesicular-arbuscular mycorrhizal fungus. Protoplasma 120, 51–60

    Google Scholar 

  • Bouligand, Y. (1965) Sur une disposition fibrillaire torsadée commune à plusieurs structures biologiques. C.R. Acad. Sci. Paris 261, 4864–4867

    Google Scholar 

  • Bouligand, Y. (1972) Twisted fibrous arrangements in biological materials and cholesteric mesophases. Tissue Cell 4, 189–217

    Google Scholar 

  • Chafe, S.C. (1970) The fine structure of the collenchyma cell wall. Planta 90, 12–21

    Google Scholar 

  • Chafe, S.C. (1974) Cell wall structure in the xylem parenchyma of Cryptomeria. Protoplasma 81, 63–76

    Google Scholar 

  • Chafe, S.C., Chauret, G. (1974) Cell wall structure in the xylem parenchyma of trembling aspen. Protoplasma 80, 129–147

    Google Scholar 

  • Chafe, S.C., Doohan, M.E. (1972) Observations on the ultrastructure of the thickened sieve cell wall in Pinus strobus L. Protoplasma 75, 67–78

    Google Scholar 

  • Chafe, S.C., Wardrop, A.B. (1972) Fine structural observations on the epidermis. I. The epidermal cell wall. Planta 107, 269–278

    Google Scholar 

  • Cox, G., Juniper, B. (1973) Electron microscopy of cellulose in entire tissue. J. Microsc. 97, 343–355

    Google Scholar 

  • Deshpande, B.P. (1976) Observations on the fine structure of plant cell walls. II. The microfibrillar framework of the parenchymatous cell wall in Cucurbita. Ann. Bot. (London) 40, 439–442

    Google Scholar 

  • Dlugosz, J., Gathercole, L.J., Keller, A. (1979) Cholesteric analogue packing of collagen fibrils in the Cuvierian tubules of Holothuria forskali (Holothuroidea, Echinodemata). Micron 10, 81–87

    Google Scholar 

  • Doohan, M.E., Newcomb, E.H. (1976) Leaf ultrastructure and δ13C values of three sea grasses from the Great Barrier Reef. Aust. J. Plant Physiol. 3, 9–23

    Google Scholar 

  • Emons, A.M.C. (1982) Microtubules do not control microfibril orientation in a helicoidal cell wall. Protoplasma 113, 85–87

    Google Scholar 

  • Emons, A.M.C., Wolters-Arts, A.M.C. (1983) Cortical microtubules and microfibril deposition in the cell wall of root bairs of Equisetum hyemale. Protoplasma 117, 68–81

    Google Scholar 

  • Erickson, R.O. (1980) Microfibrillar structure of growing plant cell walls. In: Lecture notes in biomathematics, vol. 33: Mathematical modelling in biology and ecology, pp. 192–212, Getz, W.M., ed. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Erickson, R.O. (1982) Mathematical models of plant morphogenesis. Acta Biotheor. 31, 132–151

    Google Scholar 

  • Gertel, E.T., Green, P.B. (1977) Cell growth pattern and wall microfibrillar arrangement. Plant Physiol. 60, 247–254

    Google Scholar 

  • Green, P.B. (1954) The spiral growth pattern of the cell wall in Nitella axillaris. Am. J. Bot. 41, 403–409

    Google Scholar 

  • Green, P.B. (1958) Structural characteristics of developing Nitella internodal cell walls. J. Biophys. Biochem. Cytol. 4, 505–516

    Google Scholar 

  • Green, P.B. (1960) Multinet growth in the cell wall of Nitella. J. Biophys. Biochem. Cytol 7, 289–296

    Google Scholar 

  • Grierson, J.P., Neville, A.C. (1981) Helicoidal architecture of fish eggshell. Tissue Cell 13, 819–830

    Google Scholar 

  • Grimm, I., Sachs, H., Robinson, D.G. (1976) Structure, synthesis and orientation of microfibrils. II. The effect of colchicine on the wall of Oocystis solitaria. Cytobiologie 14, 61–74

    Google Scholar 

  • Harada, H. (1965) Ultrastructure and organization of gymnosperm cell walls. In: Cellular ultrastructure of woody plants, pp. 215–233, Côté, W.A., ed. Syracuse University Press, Syracuse

    Google Scholar 

  • Hardham, A.R., Green, P.B., Lang, J.M. (1980) Reorganization of cortical microtubules and cellulose deposition during leaf formation in Graptopetalum paraguayense. Planta 149, 181–195

    Google Scholar 

  • Heath, I.B. (1974) A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J. Theor. Biol. 48, 445–449

    Google Scholar 

  • Hoffman, L.R., Hofmann, C.S. (1975) Zoospore formation in Cylindrocapsa. Can. J. Bot. 53, 439–451

    Google Scholar 

  • Jagels, R. (1973) Studies of a marine grass, Thalassia testudinum. I. Ultrastructure of the osmoregulatory leaf cells. Am. J. Bot. 60, 1003–1009

    Google Scholar 

  • Juniper, B.E., Lawton, J.R., Harris, R.J. (1981) Cellular organelles and cell-wall formation in fibers from the flowering stem of Lolium temulentum L. New Phytol. 89, 609–619

    Google Scholar 

  • Kerr, T., Bailey, I.W. (1934) The cambium and its derivative tissues. X. Structure, optical properties and chemical composition of the so-called middle lamella. J. Arnold Arbor. Harv. Univ. 15, 327–349

    Google Scholar 

  • Lang, J.M., Eisinger, W.R., Green, P.B. (1982) Effects of ethylene on the orientation of microtubules and cellulose microfibrils of pea epicotyl cells with polylamellate cell walls. Protoplasma 110, 5–14

    Google Scholar 

  • Liese, W. (1965) The warty layer. In: Cellular ultrastructure of woody plants, pp. 251–269, Côté, W.A., ed. Syracuse University Press, Syracuse

    Google Scholar 

  • Lloyd, C.W. (1982) The cytoskeleton in plant growth and development. Academic Press, New York London

    Google Scholar 

  • Meyer, K.H., Lotmar, W. (1936) L'élasticité de la cellulose. Helv. Chim. Acta 19, 68–86

    Google Scholar 

  • Mizuta, S., Wada, S. (1981) Microfibrillar structure of growing cell wall in a coenocytic green alga Boergesenia forbesii. Bot. Mag. 94, 343–353

    Google Scholar 

  • Mizuta, S., Wada, S. (1982) Effects of light and inhibitors on polylamellation and shift of microfibril orientation in Boergesenia cell wall. Plant Cell Physiol. 23, 257–264

    Google Scholar 

  • Mosse, B. (1970) Honey-coloured sessile Endogone spores. III. Wall structure. Arch. Mikrobiol. 74, 146–159

    Google Scholar 

  • Mueller, S.C., Brown, R.M. (1982a) The control of cellulose microfibril deposition in the cell wall of higher plants. I. Can directed membrane flow orient cellulose microfibrils? Indirect evidence from freeze-fractured plasma membranes of maize and pine seedlings. Planta 154, 489–500

    Google Scholar 

  • Mueller, S.C., Brown, R.M. (1983b) The control of microfibril deposition in the cell wall of higher plants. II. Freeze-fracture microfibril patterns in maize seedling tissues following experimental alteration with colchicine and ethylene. Planta 154, 501–515

    Google Scholar 

  • Neville, A.C. (1967) Chitin orientation in cuticle and its control. Adv. Insect Physiol. 4, 213–286

    Google Scholar 

  • Neville, A.C. (1975) Biology of the arthropod cuticle, pp. 1–448. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Neville, A.C. (1981) Cholesteric proteins. Mol. Cryst. Liq. Cryst. 76, 279–286

    Google Scholar 

  • Neville, A.C., Caveney, S. (1969) Scarabaeid beetle exocuticle as an optical analogue of cholesteric liquid crystals. Biol. Rev. 44, 531–562

    Google Scholar 

  • Neville, A.C., Gubb, D.C., Crawford, R.M. (1976) A new model for cellulose architecture in some plant cell walls. Protoplasma 90, 307–317

    Google Scholar 

  • Neville, A.C., Luke, B.M. (1971) A biological system producing a self-assembling cholesteric protein liquid crystal. J. Cell Sci. 8, 93–109

    Google Scholar 

  • Palevitz, B.A. (1981) The structure and development of stomatal cells. In: Stomatal physiology, pp. 1–23, Jarvis, P.G., Mansfield, T.A., eds. (Society for Experimental Biology Seminar 8). Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Parameswaran, N. (1975) Zur Wandstruktur von Sklereiden in einigen Baumrinden. Protoplasma 85, 305–314

    Google Scholar 

  • Parameswaran, N., Liese, W. (1975) On the polylamellate structure of parenchyma wall in Phyllostachys edulis Riv. Int. Assoc. Wood Anat. Bull. 4, 57–58

    Google Scholar 

  • Parameswaran, N., Liese, W. (1980) Ultrastructural aspects of bamboo cells. Cellul. Chem. Technol. 14, 587–609

    Google Scholar 

  • Parameswaran, N., Liese, W. (1981) Occurrence and structure of polylamellate walls in some lignified cells. In: Cell walls 81 (Proc. 2nd Cell Wall Meeting, Göttingen), pp. 171–188, Robinson, D.G., Quader, H., eds. Wissenschaftliche Verlagsgesellschaft, Stuttgart

    Google Scholar 

  • Parameswaran, N., Liese, W. (1982) Ultrastructural localization of wall components in wood cells. Holz Roh Werkst. 40, 145–155

    Google Scholar 

  • Parameswaran, N., Sinner, M. (1979) Topochemical studies on the wall of beech bark sclereids by enzymatic and acidic degradation. Protoplasma 101, 197–215

    Google Scholar 

  • Parker, M.L. (1979) Gravity-regulated growth of collenchymatous bundle cap-cells in the leaf sheath base of the grass Echinochloa colonum. Can. J. Bot. 57, 2399–2407

    Google Scholar 

  • Pearlmutter, N.L., Lembi, C.A. (1978) Localization of chitin in algal and fungal cell walls by light and electron microscopy. J. Histochem. Cytochem. 26, 782–791

    Google Scholar 

  • Pearlmutter, N.L., Lembi, C.A. (1980) Structure and composition of Pithophora oedogonia (Chlorophyta) cell walls. J. Phycol. 16, 602–616

    Google Scholar 

  • Pendland, J. (1979) Ultrastructural characteristics of Hydrilla leaf tissue. Tissue Cell 11, 79–88

    Google Scholar 

  • Peng, H.B., Jaffe, L.F. (1976) Cell wall formation in Pelvetia embryos. A freeze fracture study. Planta 133, 57–71

    Google Scholar 

  • Pluymaekers, H.J. (1980) Cell wall texture in root hairs of Limnobium stoloniferum. Ultramicroscopy 5, 105–106

    Google Scholar 

  • Pluymaekers, H.J. (1982) A helicoidal cell wall texture in root hairs of Limnobium stoloniferum. Protoplasma 112, 107–116

    Google Scholar 

  • Preston, R.D. (1952) The molecular architecture of plant cell walls, pp. 1–211. Chapman and Hall, London

    Google Scholar 

  • Preston, R.D. (1964) Structural plant polysaccharides. Endeavour 23, 158–159

    Google Scholar 

  • Preston, R.D. (1974) The physical biology of plant cell walls. Chapman and Hall, London

    Google Scholar 

  • Preston, R.D. (1979) Polysaccharide conformation and cell wall function. Ann. Rev. Plant Physiol. 30, 55–78

    Google Scholar 

  • Preston, R.D. (1982) The case for multinet growth in growing walls of plant cells. Planta 155, 356–363

    Google Scholar 

  • Probine, M.C., Barber, N.F. (1966) The structure and plastic properties of the cell wall of Nitella in relation to extension growth. Aust. J. Biol. Sci. 19, 439–457

    Google Scholar 

  • Probine, M.E., Preston, R.D. (1961) Cell growth and the structure and mechanical properties of the cell in internodal cells of Nitella opaca. J. Exp. Bot. 12, 261–282

    Google Scholar 

  • Ray, P.M. (1967) Radioautographic study of cell wall deposition in growing plant cells. J. Cell. Biol. 35, 659–674

    Google Scholar 

  • Reis, D. (1981) Cytochimie ultrastructurale des parois en croissance par extractions ménagées. Effects compáres du dimethylsufoxyde et de la méthylamine sur le démasquage de la texture. Ann. Sci. Nat. Bot. (Paris) 3, 121–136

    Google Scholar 

  • Reis, D., Mosiniak, M., Vian, B., Roland, J.C. (1982) Cell walls and cell shape. Changes in texture correlated with an ethylene-induced swelling. Ann. Sci. Nat. Bot. (Paris) 4, 115–133

    Google Scholar 

  • Reis, D., Vian, B., Roland, J.C. (1978) In vitro and in vivo polysaccharide assembly. Ultrastructural and cytochemical study of growing plant cell wall components. 9th Int. Congr. Elect. Microsc. Toronto, vol. 2, pp. 434–435

    Google Scholar 

  • Robinson, D.G., Herzog, W. (1977) Structure, synthesis and orientation of microfibrils. III. A survey of the action of microtubule inhibitors on microtubules and microfibril orientation in Oocystis solitaria. Cytobiologie 15, 463–474

    Google Scholar 

  • Roelofsen, P.A., Houwink, A.L. (1953) Architecture and growth of the primary wall in some plant hairs and in the Phycomyces sporangiophore. Acta Bot. Neerl. 2, 218–225

    Google Scholar 

  • Roland, J.C. (1981) Comparison of arced patterns in growing and non-growing polylamellate cell walls of higher plants. In: Cell walls '81 (Proc. 2nd Cell Wall Meeting, Göttingen), pp. 162–170, Robinson, D.G., Quader, H., eds.) Wissenschaftliche Verlagsgesellschaft, Stuttgart

    Google Scholar 

  • Roland, J.C., Mosiniak, M. (1983) On the twisting pattern, texture and layering of the secondary cell walls of limewood. Proposal of an unifying model. Int. Assoc. Wood Anat. Bull. 4, 15–26

    Google Scholar 

  • Roland, J.C., Reis, D., Mosiniak, M., Vian, B. (1982) Cell wall texture along the growth gradient of the Mung bean hypocotyl: ordered assembly and dissipative processes. J. Cell Sci. 56, 303–318

    Google Scholar 

  • Roland, J.C., Vian, B. (1979) The wall of the growing plant cell: its three dimensional organization. Int. Rev. Cytol. 61, 129–166

    Google Scholar 

  • Roland, J.C., Vian, B., Reis, D. (1977) Further observations on cell wall morphogenesis and polysaccharide arrangement during plant growth. Protoplasma 91, 125–141

    Google Scholar 

  • Sargent, C. (1978) Differentiation of the cross-fibrillar outer epidermal wall during extension growth in Hordeum vulgare L. Protoplasma 95, 309–320

    Google Scholar 

  • Sassen, M.M.A., Pluymaekers, H.J., Meekes, H.Th.H.M., De Jong-Emons, A.M.C. (1981) Cell wall texture in root hairs. In: Cell walls '81 (Proc. 2nd Cell Wall Meeting, Göttingen), pp. 189–197, Robinson, D.G., Quader, H., eds. Wissenschaftliche Verlagsgesellschaft, Stuttgart

    Google Scholar 

  • Satiat-Jeunemaître, B. (1981) Texture et croissance des parois des deux épidermes du coléoptile de mäis. Ann. Sci. Nat. Bot. (Paris) 13, 163–176

    Google Scholar 

  • Sawhney, V.K., Srivastava, L.M. (1975) Wall fibrils and microtubules in normal and gibberellic-acid-induced growth of lettuce hypotocyl cells. Can. J. Bot. 53, 824–835

    Google Scholar 

  • Schneppe, E., Stein, U., Deichgräber, G. (1978) Structure, function and development of the peristome of the moss, Rhacopilum tomentosum, with special reference to the problem of microfibril orientation by microtubules. Protoplasma 97, 221–240

    Google Scholar 

  • Seagull, R.W., Heath, I.B. (1980) The organization of cortical microtubule arrays in the radish root hair. Protoplasma 103, 205–229

    Google Scholar 

  • Steward, F.C., Mühlethaler, K. (1953) The structure and development of the cell wall in the Valoniaceae as revealed by the electron microscope. Ann. Bot. (London) 17, 295–316

    Google Scholar 

  • Spurr, A.R. (1969) A low viscosity epoxy resin embedding medium for electronmicroscopy. J. Ultrastruct. Res. 26, 31–43

    Google Scholar 

  • Takeda, K., Shibaoka, H. (1981) Effects of gibberellin and colchicine on microfibril arrangement in epidermal cell walls of Vigna angularis Ohwi and Ohashi epicotyls. Planta 151, 393–398

    Google Scholar 

  • Tang, R.C. (1973) The microfibrillar orientation in cell wall layers of Virginia pine tracheids. Wood Sci. 5, 181–186

    Google Scholar 

  • Thiery, J.P. (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J. Microsc. 6, 987–1017

    Google Scholar 

  • Vian, B. (1978) On the interpretation of twisted patterns in elongating plant cell wall: information obtained with ultracryotomy. Protoplasma 97, 379–385

    Google Scholar 

  • Vian, B., Mosiniak, M., Reis, D., Roland, J.C. (1982) Dissipative process and experimental retardation of the twisting in the growing plant cell wall. Effect of ethylene-generating agent and colchicine: a morphogenetic revaluation. Biol. Cell 46, 301–310

    Google Scholar 

  • Werbowyj, R.S., Gray, D.G. (1976) Liquid crystalline structure in aqueous hydroxypropylcellulose solutions. Mol. Cryst. Liq. Cryst. 34, 97–103

    Google Scholar 

  • Zelazny, B., Neville, A.C. (1972) Quantitative studies on fibril orientation in beetle endocuticle. J. Insect Physiol. 18, 2095–2121

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Bristol, Woodland Road, BS8 1UG, Bristol, UK

    A. C. Neville & S. Levy

Authors
  1. A. C. Neville
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Levy
    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

Neville, A.C., Levy, S. Helicoidal orientation of cellulose microfibrils in Nitella opaca internode cells: ultrastructure and computed theoretical effects of strain reorientation during wall growth. Planta 162, 370–384 (1984). https://doi.org/10.1007/BF00396750

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00396750

Key words

Search

Navigation