Skip to main content
Log in

Turgor regulation inValonia macrophysa following acute osmotic shock

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

The marine algaValonia macrophysa an inhabitant of shallow subtropical waters, is subjected to sudden dilutions of external seawater during rain showers. This study describes the mechanisms involved in turgor pressure regulation following acute hyposmotic shock. Turgor regulation is 88% effective and complete within 4 hr following hyposmotic shocks of up to −10 bar. Loss of vacuolar K+, Na+ and Cl accounts for the decrease in vacuolar osmotic pressure associated with turgor regulation. A novel mechanism of turgor regulation is exhibited byValonia macrophysa given hyposmotic shocks greater than about −4 bar. Such an osmotic shock causes cell wall tension to increase above a critical value of about 6×105 dyne/cm, whereupon the protoplasm ruptures and the cell wall stretches irreversibly at a localized site. The protoplasm rupture is suggested by (1) a large abrupt increase in K+ efflux (as measured by86Rb+), (2) a rapid decrease in turgor pressure as measured with a pressure probe, and (3) sudden depolarization of the vacuole potential. Evidence for an increase in cell wall permeability includes efflux from the vacuole of dextran (mol wt 70,000), which normally has a very low cell wall permeability, and scanning electron micrographs which show a trabeculated scar area in the cell wall. This mechanism of turgor regulation is physiologically important because 98% of the cells regained normal growth rate and turgor following acute osmotic shock.

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

References

  • Bell, A.L., Barnes, S.N., Anderson, K.L. 1969. A fixation technique for electron microscopy which provides uniformly good preservation of the tissues of a variety of marine invertebrates.Biol. Bull. 137:393

    Google Scholar 

  • Carpita, N., Sabularse, D., Montezinos, D., Delmer, D.P. 1979. Determination of the pore size of cell walls of living plant cells.Science 205:1144–1147

    Google Scholar 

  • Cram, W.J., 1976. Negative feedback regulation of transport in cells. The maintenance of turgor, volume and nutrient supply.In: Encyclopedia of Plant Physiology, New Series. U. Luttge and M.G. Pitman, editors, Vol. 2A, pp. 284–316. Springer-Verlag, New York

    Google Scholar 

  • Dainty, J. 1963. Water relations of plant cells.Adv. Bot. Res. 1:279–326

    Google Scholar 

  • Davis, R.F. 1981. Electrical properties of the plasmalemma and tonoplast inValonia ventricosa.Plant Physiol. 67:825–831

    Google Scholar 

  • Epstein, W., Schultz, S.G. 1965. Cation transport inEscherichia coli. V. Regulation of cation content.J. Gen. Physiol. 49:221–234

    Google Scholar 

  • Guggino, S., Gutknecht, J. 1980. Turgor regulation inValonia macrophysa after acute osmotic shock.In: Plant Membrane Transport: Current Conceptual Issues. R.M. Spanswick, W.J. Lucas and J. Dainty, editors. pp. 495–496. Elsevier/North Holland, New York

    Google Scholar 

  • Gutknecht, J. 1966. Sodium, potassium and chloride transport and membrane potentials inValonia ventricosa.Biol. Bull. 130:331–344

    Google Scholar 

  • Gutknecht, J. 1967. Ion fluxes and short-circuit current in internally perfused cells ofValonia ventricosa.J. Gen. Physiol. 50:1821–1834

    PubMed  Google Scholar 

  • Gutknecht J. 1968. Salt transport inValonia: Inhibition of potassium uptake by small hydrostatic pressures.Science 160:68–70

    PubMed  Google Scholar 

  • Gutknecht, J., Hastings, D.F., Bisson, M.A. 1978. Ion transport and turgor pressure regulation in giant algal cells.In: Membrane Transport in Biology. G. Giebisch, D.C. Tosteson and H.H. Ussing, editors, Vol. III, pp. 125–174. Springer-Verlag, New York

    Google Scholar 

  • Hastings, D.F. 1975. Turgor pressure regulation by the giant celled algaValonia macrophysa. Ph.D. Dissertation. University Microfilms, Ann Arbor, Michigan

    Google Scholar 

  • Hastings, D.F., Gutknecht, J. 1974. Turgor pressure regulation: Modulation of active potassium transport by hydrostatic pressure gradients.In: Membrane Transport in Plants. U. Zimmermann and J. Dainty, editors. pp. 79–83. Springer-Verlag, New York

    Google Scholar 

  • Hastings, D.F., Gutknecht, J. 1976. Ionic relations and the regulation of turgor pressure in the marine alga.Valonia macrophysa.J. Membrane Biol. 28:263–275

    Google Scholar 

  • Hellebust, J. 1976. Osmoregulation.Annu. Rev. Plant Physiol. 27:485–505

    Google Scholar 

  • Kauss, H. 1979. Osmoregulation in algae.In: Progress in Phytochemistry. L. Reinhold, J.B. Harborne and T. Swain, editors, Vol. 5, pp. 1–27. Pergamon Press, Oxford

    Google Scholar 

  • Kirst, G.O., Bisson, M.A. 1979. Regulation of turgor pressure in marine algae: Ions and low molecular weight organic compounds.Aust. J. Plant Physiol. 6:539–556

    Google Scholar 

  • Luttge, U., Higinbotham, N. 1979. Transport in Plants. p. 153. Springer-Verlag, New York

    Google Scholar 

  • Rhoads, D.B., Epstein, W. 1978. Cation transport inEscherichia coli. IX. Regulation of K transport.J. Gen. Physiol. 72:283–295

    PubMed  Google Scholar 

  • Rhoads, D.B., Woo, A., Epstein, W. 1977. Discrimination between86Rb+ and K+ byEscherichia coli.Biochim. Biophys. Acta 469:45–51

    PubMed  Google Scholar 

  • Seeman, P. 1967. Transient holes in the erythrocyte membrane during hypotonic hemolysis and stable holes in the membranes after lysis by saponin and lysolecithin.J. Cell Biol 32:55–70

    PubMed  Google Scholar 

  • Steudle, E., Zimmermann, U. 1971. Hydraulic conductivity ofValonia utricularis.Z. Naturforsch. 26b:1302–1311

    Google Scholar 

  • Steudle, E., Zimmermann, U., Lelkes, P.I. 1977. Volume and pressure effects on the potassium fluxes ofValonia utricularis.In: Transmembrane Ionic Exchanges in Plants. M. Thellier, A. Monnier, M. Demarty and J. Dainty, editors. pp. 123–132. Publications de l'Universite de Rouen, Paris

    Google Scholar 

  • Tepfer, M., Cleland, R.E. 1979. A comparison of acid-induced cell wall loosening inValonia ventricosa and in oat coleoptiles.Plant Physiol. 63:898–902

    Google Scholar 

  • Tsapis, A., Kepes, A. 1977. Transient breakdown of the permeability barrier of the membrane ofEscherichia coli upon hyposmotic shock.Biochim. Biophys. Acta 469:1–12

    PubMed  Google Scholar 

  • Zadunaisky, J.A., Degnan, K.J. 1976. Passage of sugars and urea across the isolated retina pigment epithelium of the frog.Exp. Eye Res. 23:191–196

    PubMed  Google Scholar 

  • Zimmermann, U. 1977. Cell turgor pressure regulation and turgor-pressure-mediated transport processes.In: Integration of Activity in the Higher Plant. D.H. Jennings, editor. pp. 117–154. Cambridge University Press, Cambridge

    Google Scholar 

  • Zimmermann, U. 1978. Physics of turgor and osmoregulation.Annu. Rev. Plant Physiol. 29:121–148

    Google Scholar 

  • Zimmermann, U., Steudle, E. 1974. The pressure dependence of the hydraulic conductivity, the membrane resistance and membrane potential during turgor pressure regulation inValonia utricularis.J. Membrane Biol. 16:331–352

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guggino, S., Gutknecht, J. Turgor regulation inValonia macrophysa following acute osmotic shock. J. Membrain Biol. 67, 155–164 (1982). https://doi.org/10.1007/BF01868658

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01868658

Key words

Navigation