Skip to main content
Log in

Orientation of cellulose microfibrils in cortical cells of tobacco explants

Effects of microtubule-depolymerizing drugs

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The deposition of nascent cellulose microfibrils (CMFs) was studied in the walls of cortical cells in explants of Nicotiana tabacum L. flower stalks. In freshly cut explants the CMFs were deposited in two distinct and alternating orientations — all given with respect to the longitudinal axis of the cell —, at 75° and 115°, in a left-handed (S-helix) and right-handed (Z-helix) form, respectively. The CMFs deposited in these orientations did not form uninterrupted layers, but sheets in which both orientations were present. After explantation, the synthesis of CMFs and their deposition in bundles continued. New orientations occurred within 6 h. After 6 h a new sheet was deposited, with orientations of 15° (S-helix) and 165° (Z-helix). The changes could be seen as sudden bends in individual CMFs or in small bundles of CMFs. In the next stage, more CMFs were deposited with these new orientations and the bundles became larger. New orientations arose by a shift towards more longitudinal directions, starting from either the S-helix or the Z-helix form. It was only after an almost longitudinal orientation was reached that the CMFs were deposited in two opposing directions again and a new sheet was formed. Neither colchicine nor cremart influenced the changes in CMF deposition. It is concluded that microtubules do not control CMF deposition in cortical cells of tobacco explants; control of CMF deposition and microtubule orientation occurs by factors related to cell polarity.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

CMF:

cellulose microfibril

MT:

microtubule

References

  • Bergfeld, R., Speth, V., Schöpfer, P. (1988) Reorientation of microfibrils and microtubules at the outer epidermal wall of maize coleoptiles during auxin-mediated growth. Bot. Acta 101, 57–67

    Google Scholar 

  • Derksen, J. (1986) Cytoskeletal control of cellulose microfibril deposition. In: Cell walls 1986 (Proc. 4th Cell Wall Meeting, Paris 1986), pp. 34–37, Vian, B., Reiss, D., Goldberg, R., eds. Groupe Paris, France

    Google Scholar 

  • Derksen, J., Wilms, F.H.A., Pierson, E.S. (1990) The plant cytoskeleton: Its significance in plant development. Acta Bot. Neerl. 38, 1–18

    Google Scholar 

  • Eisinger, W., Croner, L.J., Taiz, L. (1983) Ethylene-induced lateral expansion in etiolated pea stems. Kinetics, cell wall synthesis and osmotic potential. Plant Physiol. 73, 407–412

    Google Scholar 

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

    Google Scholar 

  • Emons, A.M.C. (1985) Plasma membrane rosettes in root hairs of Equisetum hyemale. Planta 163, 350–359

    Google Scholar 

  • Emons, A.M.C. (1989) Helicoidal microfibril deposition in a tipgrowing cell and microtubule alignment during tip morphogenesis: a dry-cleaving and freeze substitution study. Can. J. Bot., in press

  • Giddings, T.H., Steahelin, L.A. (1988) Spatial relationship between microtubules and plasma-membrane rosettes during the deposition of primary wall microfibrils in Closterium sp. Planta 173, 22–30

    Google Scholar 

  • Green, P.B. (1980) Organogenesis. A biophysical view. Annu. Rev. Plant Physiol. 31, 51–82

    Google Scholar 

  • Hardham, A.R. (1982) Regulation of polarity in tissues and organs. In: The cytoskeleton in plant growth and development, pp. 377–403, Lloyd, C.W., ed. Academic Press, London

    Google Scholar 

  • Hayano, S., Itoh, T., Brown, R.M., jr. (1988) Orientation of microtubules during regeneration of cell wall in selected giant marine algae. Plant Cell Physiol. 29, 785–793

    Google Scholar 

  • Hepler, P.K. (1985) The plant cytoskeleton. In: Botanical microscopy, pp. 233–262, Robards, A.W., ed. Oxford University Press, Oxford

    Google Scholar 

  • Herth, W. (1985) Plant cell wall formation. In: Botanical microscopy, pp. 285–310, Robards, A.W., ed. Oxford University Press, Oxford

    Google Scholar 

  • Hogetsu, T. (1986) Orientation of wall microfibril deposition in root cells of Pisum sativum L. var. Alaska. Plant Cell Physiol. 27, 947–951

    Google Scholar 

  • Imaseki, H. (1985) Ethylene. In: Chemistry of plant hormones, pp. 249–264, Takahashi, N., ed. CRC Press, Inc., Boca Raton

    Google Scholar 

  • Iwata, K., Hogetsu, T. (1989) Orientation of wall microfibrils in Avena coleoptiles and mesocotyls and in Pisum epicotyls. Plant Cell Physiol. 30, 749–757

    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 

  • Lloyd, C.W. (1984) Towards a dynamic helical model for the influence of microtubules on wall patterns in plants. Int. Rev. Cytol. 86, 1–35

    Google Scholar 

  • Mita, T., Shibaoka, H. (1984) Gibberellin stabilizes microtubules in onion leaf sheath cells. Protoplasma 119, 100–109

    Google Scholar 

  • Mizuta, S. (1985) Assembly of cellulose synthesizing complexes on the plasma membrane of Boodlea coacta. Plant Cell Physiol. 26, 1443–1453

    Google Scholar 

  • Mueller, S.C., Brown, R.M., Jr. (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., Jr. (1982b) The control of cellulose 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 

  • Murashige, T., Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 373–397

    Google Scholar 

  • Okuda, K., Mizuta, S. (1987) Modification in cell shape unrelated to cellulose microfibril orientation in growing thallus cells of Cheatomorpha moniligera. Plant Cell Physiol. 28, 461–473

    Google Scholar 

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

    Google Scholar 

  • Preston, R.D. (1988) Cellulose-microfibril-orienting mechanisms in plant cell walls. Planta 174, 67–74

    Google Scholar 

  • Quader, H. (1986) Cellulose microfibril orientation in Oocystis solitaria: proof that microtubules control the alignment of terminal complexes. J. Cell Sci. 83, 223–234

    Google Scholar 

  • Quader, H., Wagenbreth, I., Robinson, D.G. (1978) Structure, synthesis and orientation of microfibrils. V. On the recovery of Oocystis solitaria from microtubule inhibitor treatment. Cytobiol 18, 39–51

    Google Scholar 

  • Quader, H., Deichgraber, G., Schnepf, E. (1986) The cytoskeleton in Cobaea seed hair development: Patterning during cell-wall differentiation. Planta 168, 1–10

    Google Scholar 

  • Ridge, I. (1973) The control of cell shape and rate of cell expansion by ethylene: effects on microfibril orientation and cell wall extensibility in etiolated peas. Acta Bot. Neerl. 22, 144–158

    Google Scholar 

  • Roberts, I.N., Lloyd, C.W., Roberts, K. (1985) Ethylene-induced microtubule reorientation: mediation by helical arrays. Planta 164, 439–447

    Google Scholar 

  • Robinson, D.G., Quader, H. (1982) The microtubule-microfibril syndrome. In: The cytoskeleton in plant growth and development, pp. 109–126, Lloyd, C.W., ed. Academic Press, London

    Google Scholar 

  • Roelofsen, P.A. (1951) Orientation of cellulose microfibrils in the cell wall of growing cotton hairs and its bearing on the physiology of cell wall growth. Biochim. Biophys. Acta 7, 45–53

    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., Reis, D., Vian, B., Satiat-Jeunemaitre, B., Mosiniak, M. (1979) Morphogenesis of plant cell walls at the supramolecular level: Internal geometry and versatility of helicoidal expression. Protoplasma 140, 75–91

    Google Scholar 

  • Ryser, U. (1985) Cell wall biosynthesis in differentiating cotton fibres. Eur. J. Cell Biol. 39, 236–256

    Google Scholar 

  • Sassen, M.M.A., Wolters-Arts, A.M.C. (1986) Cell wall texture and cortical microtubules in growing staminal hairs of Tradescantia virginiana. Acta Bot. Neerl. 35, 351–360

    Google Scholar 

  • Sassen, M.M.A., Traas, J.A., Wolters-Arts, A.M.C. (1985) Deposition of cellulose microfibrils in cell walls of root hairs. Eur. J. Cell Biol. 1371, 21–26

    Google Scholar 

  • Schnepf, E. (1986) Cellular polarity. Annu. Rev. Plant Physiol. 37, 23–47

    Google Scholar 

  • Smulders, M.J.M. (1989) Auxin regulation of flower bud formation in tobacco explants. Role of concentration and sensitivity. Thesis, University of Nijmegen, The Netherlands

    Google Scholar 

  • Traas, J.A., Derksen, J. (1989) Microtubules and cellulose microfibrils in plant cells: simultaneous demonstration in dry cleaved preparations. Eur. J. Cell Biol. 48, 159–164

    Google Scholar 

  • Traas, J.A., Braat, P., Derksen, J.W. (1984) Changes in microtubule arrays during the differentiation of cortical root cells of Raphanus stivus. J. Cell Biol. 34, 229–238

    Google Scholar 

  • Traas, J.A., Braat, P., Emons, A.M.C., Meekes, H., Derksen, J. (1985) Microtubules in root hairs. J. Cell Sci. 76, 303–320

    Google Scholar 

  • Tran Thanh Van, K. (1977) Regulation of morphogenesis. In: Plant tissue culture and its bio-technological application, pp. 367–385, Barz, W., Reinhard, E., Zenk, M.H., eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Williams, E.G., Maheswaran, G. (1986) Somatic embryogenesis: Factors influencing coordinated behaviour of cells as an embryogenic group. Ann. Bot. 57, 443–462

    Google Scholar 

  • Wilms, F.H.A., Derksen, J. (1988) Reorganization of cortical microtubules during cell differentiation in tobacco explants. Protoplasma 146, 127–132

    Google Scholar 

  • Wilms, F.H.A., Sassen, M.M.A. (1987) Origin and development of floral buds in tobacco explants. New Phytol. 105, 57–65

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

We thank Professor M.M.A. Sassen and Dr. G.W.M. Barendse (Department of Experimental Botany, University of Nijmegen, Nijmegen, The Netherlands) for helpful discussions and Mrs. A. Kemp for her assistance in the ethylene experiments.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wilms, F.H.A., Wolters-Arts, A.M.C. & Derksen, J. Orientation of cellulose microfibrils in cortical cells of tobacco explants. Planta 182, 1–8 (1990). https://doi.org/10.1007/BF00239976

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00239976

Key words

Navigation