SpringerLink
Log in

Effects of microtubule agents on the spatial and electrical properties of the plasma membrane inChara corallina

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The freshwater algaChara corallina Klein ex Willd., em. R.D.W. (=C. australis R.Br.) develops alternating outward (acid) and inward (alkaline) current areas on its surface when illuminated. Exposure of cells to vinblastine, colchicine, or oryzalin caused a reduction in and a shifting of this extracellular current pattern. Removal of these agents from the bathing media resulted in regeneration of the initial current profile. Because these agents all affect tubulin, microtubules may be responsible for orchestrating the transmembrane currents responsible for the acid and alkaline banding phenomenon. Analysis of the membrane potential showed a fast depolarization after vinblastine exposure; however, analysis of the current-voltage curve did not show a change in membrane conductance. A 30-min colchicine treatment decreased the conductance of the plasma membrane with either an hyperor a depolarization in the membrane potential. In contrast, although a 9-h exposure to oryzalin caused a major reduction in the extra-cellular current pattern, only minor changes were observed in the membrane potential and conductance. However, in the presence of oryzalin, the time constants in the light response of the membrane potential increased over this 9-h period. Collectively, these results implicate an involvement of microtubules in spatial control of plasma-membrane transport events inC. corallina.

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
EUR 32.99 /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 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

Abbreviations

I/V:

current voltage curve

CPW/B:

artificialChara pond water

References

  • Bajer, A.S., Molé-Bajer, J. (1986) Drugs with colchicine-like effects that specifically disassemble plant but not animal microtubules. Ann. N.Y. Acad. Sci.466, 767–784

    CAS  PubMed  Google Scholar 

  • Beilby, M.J. (1984) Current-voltage characteristics of the proton pump atChara plasmalemma. I. pH dependence. J. Membr. Biol.81, 113–125

    Google Scholar 

  • Bernier-Valentin, F., Aunis, D., Rousset, B.J. (1983) Evidence for tubulin-binding sites on cellular membranes: plasma membranes, mitochondrial membranes, and secretory granule membranes. Cell Biol.97, 209–216

    CAS  Google Scholar 

  • Fisahn, J., Lucas, W.J. (1990a) Application of asymmetric alternating voltage pulse series for investigation of the action potential inChara. Plant Cell Physiol.31, 155–157

    Google Scholar 

  • Fisahn, J., Lucas, W.J. (1990b) Inversion of extracellular current and axial voltage profile inChara andNitella. J. Membr. Biol.113, 1–8

    Google Scholar 

  • Fisahn, J., Mikschl, E., Hansen, U.-P. (1986a) Separate oscillations of the electrogenic pump and of a K+ channel inNitella as revealed by simultaneous measurement of membrane potential and of resistance. J. Exp. Bot.37, 34–47

    CAS  Google Scholar 

  • Fisahn, J., Hansen, U.-P., Gradmann, D.J. (1986b) Determination of charge, stoichiometry and reaction constants from I/V curve studies on a K+ transporter inNitella. J. Membr. Biol.94, 245–252

    CAS  Google Scholar 

  • Fisahn, J., McConnaughey, T., Lucas, W.J. (1989) Oscillations in extracellular current, external pH and membrane potential and conductance in the alkaline bands ofNitella andChara. J. Exp. Bot.40, 1185–1193

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hansen, U.-P., Gradmann, D., Sanders, D., Slayman, C.L. (1981) Interpretation of current-voltage relationships for “active” ion transport systems: I. Steady-state reaction-kinetic analysis of class-I mechanisms. J. Membr. Biol.63, 165–190

    CAS  PubMed  Google Scholar 

  • Hashizume, T., Akiba, S., Sato, T., Fujii, T., Watanabe, S., Sasaki, J. (1988) Vinblastine inhibits platelet aggregation by a microtubule-independent mechanism, probably by its perturbing action on the plasma membrane. Thromb. Res.50, 181–190

    Article  CAS  PubMed  Google Scholar 

  • Hucho, F., Hilgendorf, R. (1989) The selectivity filter of a ligandgated ion channel. The helix-M2 model of the ion channel of the nicotinic acetylcholine receptor. FEBS Lett.257, 17–23

    Article  CAS  PubMed  Google Scholar 

  • Keifer, D.W., Lucas, W.J. (1982) Potassium channels inChara corallina: control and interaction with the electrogenic H+ pump. Plant Physiol.69, 781–788

    CAS  Google Scholar 

  • Lloyd, C.W. (1987) The plant cytoskeleton: the impact of fluorescence microscopy. Annu. Rev. Plant Physiol.38, 119–139

    CAS  Google Scholar 

  • Lucas, W.J. (1975) The influence of light intensity on the activation and operation of the hydroxyl efflux system ofChara corallina. J. Exp. Bot.26, 347–360

    CAS  Google Scholar 

  • Lucas, W.J. (1982) Mechanism of acquisition of exogenous bicarbonate by internodal cells ofChara corallina. Planta156, 181–192

    Article  CAS  Google Scholar 

  • Lucas, W.J. (1983) Photosynthetic assimilation of exogenous HCO3/- by aquatic plants. Annu. Rev. Plant. Physiol.34, 71–104

    Article  CAS  Google Scholar 

  • Lucas, W.J., Nuccitelli, R. (1980) HCO3/- and OH- transport across the plasmalemma ofChara corallina: spatial resolution obtained using extracellular vibrating probe. Planta150, 120–131

    Article  CAS  Google Scholar 

  • Lucas, W.J., Spanswick, R.M., Dainty, J. (1978) HCO3/- influx across the plasmalemma ofChara corallina: physiological and biophysical influence of 10 mM K+. Plant Physiol.61, 487–493

    CAS  Google Scholar 

  • Luduena, R.F., Anderson, W.H., Prasad, V., Jordan, M.A., Ferrigni, K.C., Roach, M.C., Horowitz, P.M., Murphy, D.B., Fellous, A. (1986) Interactions of vinblastine and maytansine with tubulin. Ann. N.Y. Acad. Sci.466, 718–732

    CAS  PubMed  Google Scholar 

  • Morejohn, L.C., Fosket, D.E. (1984) Taxol-induced rose microtubule polymerization in vitro and its inhibition by colchicine. J. Cell Biol.99, 141–147

    Article  CAS  PubMed  Google Scholar 

  • Niggli, V., Burger, M.M. (1987) Interaction of the cytoskeleton with the plasma membrane. J. Membr. Biol.100, 97–121

    CAS  PubMed  Google Scholar 

  • Nuccitelli, R. (1986) A two-dimensional vibrating probe with a computerized graphics display. In: Ionic currents in development, pp. 13–20, Nuccitelli, R., ed. Liss, New York

    Google Scholar 

  • Ribbi-Jaffe, A., Apitz-Castro, R. (1979) The effect of colchicine on human blood platelets under conditions of short-term incubation. Biochem. J.178, 449–454

    CAS  PubMed  Google Scholar 

  • Richmond, P.A. (1983) Patterns of cellulose microfibril deposition and rearrangement inNitella: in vivo analysis by a birefringence index. J. Appl. Polymer. Sci.: Applied Polymer Symp.37, 107–122

    CAS  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 inOocystis solitaria. Cytobiologie15, 463–474

    CAS  Google Scholar 

  • Spanswick, R.M. (1981) Electrogenic ion pumps. Annu. Rev. Plant Physiol.32, 267–289

    Article  CAS  Google Scholar 

  • Tyerman, S.D., Findlay, G.P., Paterson, G.J. (1986) Inward membrane current inChara inflata: Effects of pH, Cl--channel blockers and NH4/-, and significance for the hyperpolarized state. J. Membr. Biol.89, 153–161

    CAS  Google Scholar 

  • Upadhyaya, M.K., Noodén, L.D. (1980) Mode of dinitroaniline herbicide action. II. Characterization of [14C]oryzalin uptake and binding. Plant Physiol.66, 1048–1052

    CAS  Google Scholar 

  • Vassilev, P.M., Kanazirska, M.P., Tien, H.T. (1986) Microtubule-dependent membrane interactions studied in two types of double bilayer membrane systems. Bioelectrochem. Bioenerg.15, 395–406

    Article  CAS  Google Scholar 

  • Weerdenburg, C., Seagull, R.W. (1988) The effects of taxol and colchicine on microtubule and microfibril arrays in elongating plant cells in culture. Can. J. Bot.66, 1707–1716

    Google Scholar 

  • Williamson, R.F., Perkin, J.L., McCurdy, D.W., Craig, S., Hurley, U.A. (1986) Production and use of monoclonal antibodies to study the cytoskeleton and other components of the cortical cytoplasm ofChara. Eur. J. Cell Biol.41, 1–8

    Google Scholar 

  • Zisapel, N., Levi, M., Gozes, I. (1980) Tubulin: an integral protein of mammalian synaptic vesicle membranes. J. Neurochem.34, 26–32

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, University of California, 95616, Davis, CA, USA

    Joachim Fisahn & William J. Lucas

Authors
  1. Joachim Fisahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William J. Lucas
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This research was supported by National Science Foundation grant DCB-88-16077.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fisahn, J., Lucas, W.J. Effects of microtubule agents on the spatial and electrical properties of the plasma membrane inChara corallina . Planta 182, 506–512 (1990). https://doi.org/10.1007/BF02341025

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02341025

Key words

Search

Navigation