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Cellulose-microfibril-orienting mechanisms in plant cells walls

Abstract

A brief review is given of the changing views over the years, as knowledge of wall structure has developed, concerning the mechanism whereby cellulose chains may be oriented. This leads to an examination of current concepts, particularly those concerning microtubules. It is shown that none of the mechanisms suggested whereby microtubules might cause orientation of cellulose microfibrils is consistent with the known range of molecular architectures found in plant cell walls. It is further concluded that any mechanism which necessitates an indissoluble link between the plasmalemma and the cellulose-synthesising complex at the tip of a microfibril is unacceptable. A new proposal is presented in which it is speculated that both microtubules and microfibrils are oriented by a mechanism separate from both. It is shown that if two vectors are contemplated, one parallel to cell length and one at right angles, and a sensor exists on the plasmalemma surface which responds to changes in the vectors, then all known wall structures may be explained. The possible nature of the vectors and the sensor are considered.

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References

  1. Astbury, W.T., Bell, F.O. (1941) Nature of the intramolecular fold in alpha-keratin and alpha-myosin. Nature 147, 696–699

  2. Astbury, W.T., Preston, R.D. (1940) The structure of the cell wall in some species of the filamentous green alga Cladophora. Proc. R. Soc. London Ser. B 129, 54–76

  3. Berlin, R.D., Oliver, J.M., Ukena, T.E., Yin, H.H. (1974) Control of cell surface topography. Nature 247, 45–46

  4. Castle, E.S. (1937) Membrane tension and orientation of structure in the plant cell wall. J. Cell. Comp. Physiol. 10, 113–121

  5. Chafe, S.C. (1978) On the mechanism of cell wall microfibrillar orientation. Wood Sci. Technol. 12, 203–219

  6. Estridge, M. (1977) Polypeptides similar to the α and β subunits of tubulin are exposed on the neuronal surface. Nature 268, 60–63

  7. Frei, E., Preston, R.D. (1961) Cell wall organisation and cell growth in the filamentous green algae Cladophora and Chaetomorpha I. The basic structure. Proc. R. Soc. London Ser. B 154, 70–94

  8. Frey-Wyssling, A., Mühlethaler, K., Wyckoff, R.W.G. (1948) Mikrofibrillenbau der pflanzlichen Zellwand. Experientia 4, 475–477

  9. Gahmber, C.G. (1977) Membrane glycoproteins and glycolipids: Structure, localisation and function of the carbohydrate. In: Membrane structure and function, pp. 127–154, Finean, J.B., Mitchell, R.H., eds. Elsevier, New York

  10. Gardner, K.H., Blackwell, J. (1974) The structure of native cellulose. Biopolymers 13, 1975–1984

  11. Gompertz, B. (1977) The plasma membrane: models for structure and function. Academic Press, London New York

  12. 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

  13. Gunning, B.E.S., Hardham, A.R. (1982) Microtubules. Annu. Rev. Plant Physiol. 33, 651–698

  14. Hepler, P.K. (1981) Morphogenesis of tracheary elements and guard cells. In: Cytomorphogenesis in plants (Int. Biol. Monogr. vol. 8), pp. 327–347, Kiermayer, O., ed. Academic Press, New York

  15. Hol, W.G.J., Halie, M.L., Sanders, M.C. (1981) Dipoles of the α-helix and β-sheet: their role in protein folding. Nature 294, 532–536

  16. Ledbetter, M.C., Porter, K. (1963) A “microtubule” in plant cell fine structure. J. Cell Biol. 19, 239–250

  17. Lloyd, C.W. (1984) Toward a dynamic helical model for the influence of microtubules on cell wall patterns in plants. Int. Rev. Cytol. 86, 1–51

  18. Martens, P. (1940) Mouvement protoplasmique et relief de la parois cellulaire. La Cellule 48, 249–258

  19. Mita, T., Shibaoka, H. (1983) Changes in microtubules in onion leaf sheath cells during bulb development. Plant Cell Physiol. 24, 109–117

  20. Moor, H., Mühlethaler, K. (1963) Fine structure in frozenetched yeast cells. J. Cell Biol. 17, 609–628

  21. Nicolai, M.F.E., Frey-Wyssling, A. Über den Feinbau der Zellwand von Chaetomorpha. Protoplasma 30, 401–413

  22. Nicolai, M.F.E., Preston, R.D. (1953) Cell wall studies in the Chlorophyceae. II. A preliminary study of the effect of constant illumination on wall structure in Cladophora rupestris. Proc. Roy. Soc. London Ser. B 141, 407–419

  23. Nicolai, M.F.E., Preston, R.D. (1959) Cell wall studies in the Chlorophyceae. III. Differences in structure and development in the Cladophorales. Proc. Roy. Soc. London Ser. B 151, 244–254

  24. Nieduszinski, I.A., Atkins, E.D.T. (1970) Preliminary study of algal celluloses. I. X-ray intensity data. Biochim. Biophys. Acta 222, 109–118

  25. Pizzi, A., Eaton, N. (1985) The structure of cellulose by conformational analysis. 2. The cellulose polymer chain. J. Macromol. Sci. Chem. 22(1), 105–114

  26. Preston, R.D. (1934) The organisation of the walls of conifer tracheids. Philos. Trans. R. Soc. London Ser. B 224, 131–174

  27. Preston, R.D. (1941) “Crossed fibrillar” structure of plant cell walls. Nature 147, 710

  28. Preston, R.D. (1964) Structural and mechanical aspects of plant cell walls with particular reference to synthesis and growth. In: The formation of wood in forest trees, pp. 169–201, Zimmermann, M.H., ed. Academic Press, New York London

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

  30. Preston, R.D., Astbury, W.T. (1937) The structure of the wall of the green alga Valonia ventricosa. Proc. R. Soc. London Ser. B 122, 76–97

  31. Preston, R.D., Goodman, R.W. (1968) Structural aspects of cellulose microfibril biosynthesis. J. R. Microsc. Soc. 88, 513–522

  32. Preston, R.D., Nicolai, M.F.E., Reed, R., Millard, A. (1948) An electron microscope study of cellulose in the wall of Valonia ventricosa. Nature 162, 957–959

  33. Preston, R.D., Singh, K. (1950) The fine structure of bamboo fibres I. Optical properties and X-ray data. J. Exp. Bot. 1, 214–232

  34. Preston, R.D., Wardrop, A.B. (1949) The fine structure of the wall of the conifer tracheid IV. Dimensional relationships in the outer layer of the secondary wall. Biochim. Biophys. Acta 3, 585–592

  35. Quader, H., Deichgräber, G., Schnepf, E. (1987) The cytoskeleton of Cobaea seed hairs: patterning during cell wall development. Planta 168, 1–10

  36. Quader, H., Herth, W., Schnepf, E. (1987) Cytoskeletal elements in cotton seed hair developed in vitro: their possible regulatory role in cell wall organisation. Protoplasma 137, 56–61

  37. Quatrano, R.S. (1978) Development of cell polarity. Annu. Rev. Plant Physiol. 29, 487–510

  38. Robinson, D.G. (1985) Plant membranes. John Wiley and Sons, London

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

  40. Sarko, A., Muggli, R. (1974) Packing analysis of carbohydrates and polysaccharides IV: Valonia cellulose and cellulose II. Macromolecules 7, 486–492

  41. Srivistava, L.M., Sawhney, V.K., Bonettemaker, M. (1977) Cell growth, wall deposition and correlated fine structure of colchicine treated lettuce hypocotyl cells. Can. J. Bot. 55, 902–917

  42. Stern, F., Stout, H.P. (1954) Morphological relations in cellulose fibre cells. J. Text. Inst. 45, 1896–1911

  43. Sugiama, J., Harada, H., Fujiyoshi, Y., Ueda, N. (1985) Observations of cellulose microfibrils in Valonia macrophysa by high resolution electron microscopy. Mokusai Gakkaishi 31(2), 61–64

  44. Van Iterson, G., Jr (1937) A few observations on the hairs of Tradescantia virginica. Protoplasma 27, 190–211

  45. Wardrop, A.B. (1964) The structure and formation of the cell wall in xylem. In: The formation of wood in forest trees, pp. 87–134, Zimmermann, M.H., ed. Academic Press, New York London

  46. Weisenseel, M.H., Kicherer, R.M. (1981) Ionic currents as control mechanisms in cytomorphogenesis. In: Cytomorphogenesis in plants (Cell Biol. Monogr. vol. 8), pp. 379–399, Kiermayer, O., ed. Academic Press, New York

  47. Willison, J.H.M. (1982) Microfibril-tip growth and the developments of pattern in cell walls. In: Cellulose and other natural polymer systems, pp. 105–125, Brown, R.M., Jr, ed. Plenum Press, London New York San Francisco

  48. Willison, J.H.M., Brown, R.M., Jr (1978) Cell wall structure and deposition in Glaucocystis. J. Cell Biol. 77, 103–119

  49. Wunderlich, F., Müller, R., Speth, V. (1973) Direct evidence for a colchicine-induced impairment in the mobility of membrane components. Science 182, 1136–1138

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Preston, R.D. Cellulose-microfibril-orienting mechanisms in plant cells walls. Planta 174, 67–74 (1988). https://doi.org/10.1007/BF00394875

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Key words

  • Cellulose (chain orientation)
  • Cell wall (structure)
  • Microfibril (orientation)
  • Microtubule (orientation)