Planta

, Volume 179, Issue 4, pp 421–427 | Cite as

Light-promoted changes in apoplastic K+ activity in the Samanea saman pulvinus, monitored with liquid membrane microelectrodes

  • Cara Zucker Lowen
  • Ruth L. Satter
Article

Abstract

The movement of Samanea saman (Jacq.) Merrill leaflets is a consequence of the re-distribution of K+ and anions between motor cells on opposite sides of the pulvinus. We used a K+-sensitive microelectrode to study dynamic changes in K+ transport through motor-cell membranes during and immediately after change in illumination. Potassium-ion-sensitive and reference microelectrodes were inserted into extensor or flexor tissue of a whole pulvinus in white light (WL). A brief pulse of red light (RL) followed by darkness (D) (a) increased K+ activity in the extensor apoplast, indicating K+ release by the protoplast; and (b) decreased K+ activity in the flexor apoplast, indicating K+ uptake by the protoplast. White light after 35–40 min D reversed K+ activity in the extensor apoplast to approximately its original value. Blue light substituted partially for WL in this regard. Potassium-ion activity in the flexor apoplast reverted to approximately its original value after 2 h, with or without white illumination. Our data support the hypothesis that K+ efflux from extensor cells and K+ uptake by flexor cells following a WL→RL→D transition occurs by way of K+ channels.

Key words

Apoplastic potassium activity Light effect on potassium fluxes Potassium channels Pulvinus Samanea 

Abbreviations

L

light

WL

white light

RL

red light

BL

blue light

D

darkness

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Assmann, S.M., Simoncini, L., Schroeder, J.I. (1985) Blue light activates electrogenic ion pumping in guard cell protoplasts of Vivia faba. Nature 318, 285–287Google Scholar
  2. Blatt, M.R. (1985). Extracellular potassium activity in attached leaves and its relation to stomatal function. J. Exp. Bot. 36, 240–251Google Scholar
  3. Borthwick, H.A. (1972) The biological significance of phytochrome. In: Phytochrome, pp. 27–44, Mitrakos, K., Shropshire, W., Jr., eds. Academic Press, LondonGoogle Scholar
  4. Bowling, D.J.F. (1987) Measurement of the apoplastic activity of K+ and Cl- in the leaf epidermis of Commelina communis in relation to stomatal activity. J Exp. Bot. 38, 1351–1355Google Scholar
  5. Campbell, D.T., Hahin, R. (1984) Altered sodium and gating current kinetics in frog skeletal muscle caused by low external pH. J. Gen. Physiol. 84, 771–786Google Scholar
  6. Campbell, N.A., Satter, R.L., Garber, R.C. (1981) Apoplastic transport of ions in the motor organ of Samanea. Proc. Natl. Acad. Sci. USA 78, 2981–2984Google Scholar
  7. Felle, H., Bertl, A. (1986) The fabrication of H+-selective liquid-membrane microelectrodes for use in plant cells. J. Exp. Bot. 37, 1416–1428Google Scholar
  8. Fondeville, J.C., Schneider, M.J., Borthwick, H.J., Hendricks, S.B. (1967) Photocontrol on Mimosa pudica L. leaf movement. Planta 75, 228–238Google Scholar
  9. Freudling, C., Starrach, N., Flach, D., Gradmann, D., Mayer, W.-E. (1988) Cell walls as reservoirs of potassium ions for reversible volume changes of pulvinar motor cells during rhythmic leaf movements. Planta 175, 193–203Google Scholar
  10. Gorton, H. (1987) Water relations in pulvini from Samanea saman. I. Intact pulvini. Plant Physiol 83, 945–950Google Scholar
  11. Iglesias, A., Satter, R.L. (1983) H+ fluxes in excised Samanea motor tissuee. I. Promotion by light. Plant Physiol. 72, 564–569Google Scholar
  12. Kiyosawa, K. (1979) Unequal distribution of potassium and anions in Phaseolus pulvini. Plant Cell Physiol. 20, 1621–1634Google Scholar
  13. Kumon, K., Tsurumi, S. (1984) Ion efflux from pulvinar cells during slow downward movement of the petiole of Mimosa pudica L. induced by photostimulation. J. Plant Physiol. 115, 439–443Google Scholar
  14. Lee, Y., Satter, R.L. (1989) Effects of white, blue, red light and darkness on pH of the apoplast in the Samanea pulvinus. Planta 178, 31–40Google Scholar
  15. Lucas, W.J., Kochian, L.V. (1986) Ion transport processes in corn roots: an approach utilizing microelectrode technique. In: Advanced agricultural instrumentation, pp. 402–405, Gensler, W., ed. Martinus Nijhoff, The HagueGoogle Scholar
  16. Mayer, W. (1977) Kalium-und Chloridverteilung im Laminargelenk von Phaseolus coccineus L. während der circadianen Blattbewegung im tagesperiodischen Licht-Dunkenwechsel. Z. Pflanzenphysiol. 83, 127–135Google Scholar
  17. Moran, N., Ehrenstein, G., Iwasa, K., Mischke, C., Bare, C., Satter, R.L. (1988) Potassium channels in motor cells of Samanea saman. A patch clamp study. Plant Physiol. 88, 643–648Google Scholar
  18. Nobel, P.S. (1974) Introduction to biophysical plant physiology. Freeman, San FranciscoGoogle Scholar
  19. Pietrobon, D., Prod'hom, B., Hess, P. (1988) Conformational changes associated with ion permeation in L-type calcium channels. Nature 332, 373–376Google Scholar
  20. Racusen, R.H., Satter, R.L. (1975) Rhythmic and phytochrome-regulated changes in transmembrane potential in Samanea pulvini. Nature 255, 408–410Google Scholar
  21. Raymond, L., Slatin, S.L., Finkelstein, A. (1985) Channels formed by colicin E1 in planar lipid bilayers are large and exhibit pH-dependent ion selectivity. J. Membr. Biol. 84, 173–181Google Scholar
  22. Robinson, R.A., Stokes, R.H. (1959) Electrolyte solutions, 2nd edn. Batterworth, LondonGoogle Scholar
  23. Satter, R.L. (1979) Leaf movements and tendril curling. In: Encyclopedia of plant physiology, N.S., vol. 7. Physiology of movements, pp. 442–484, Haupt, W., Feinleib, m.E., eds. Springer, Berlin Heidelberg New YorkGoogle Scholar
  24. Satter, R.L., Galston, A.W. (1981) Mechanisms of control of leaf movements. Annu. Rev. Plant Physiol. 32, 83–110Google Scholar
  25. Satter, R.L., Geballe, G.T., Applewhite, P.B., Galston, A.W. (1974a) Potassium flux and leaf movement in Samanea saman. I. Rhythmic movement. J. Gen Physiol. 64, 413–430Google Scholar
  26. Satter, R.L., Geballe, G.T., Galston, A.W. (1974b) Potassium flux and leaf movement in Samanea saman. II. Phytochrome controlled movement. J. Gen. Physiol. 64, 431–442Google Scholar
  27. Satter, R.L., Guggino, S.E., Lonergan, T.A., Galston, A.W. (1981) The effects of blue and far red light on rhythmic leaflet movements in Albizzia and Samanea. Plant Physiol. 67, 965–968Google Scholar
  28. Satter, R.L., Marinoff, P., Galston, A.W. (1970) Phytochrome controlled nyctinasty in Albizzia julibrissin. II. Potassium flux as a basis for leaflet movement. Am. J. Bot. 57, 916–926Google Scholar
  29. Satter, R.L., Schrempf, M., Chaudhri, J., Galston, A.W. (1977) Phytochrome and circadian clocks in Samanea: rhythmic redistribution of potassium and chloride within the pulvinus during long dark periods. Plant Physiol. 59, 231–235Google Scholar
  30. Satter, R.L., Xu, Y., DePass, A. (1987) Effects of temperature on H+ secretion and uptake by excised flexor cells during dark-induced closure of Samanea leaflets. Plant Physiol. 85, 850–855Google Scholar
  31. Schroeder, J.I., Raschke, K., Neher, E. (1987) Voltage dependence of K+ channels in guard-cell protoplasts. Proc. Natl. Acad. Sci. USA 84, 4108–4112Google Scholar
  32. Scott, B.I.H. Gulline, H.F. (1975) Membrane changes in a circadian system. Nature 254, 69–70Google Scholar
  33. Senger, H., (1984) Cryptochrome, some terminological thoughts. In: Blue light effects in biological systems, pp. 72–80, Senger, H., ed. Springer, Berlin Heidelberg New YorkGoogle Scholar
  34. Sweet, H.C., Hillman, W.S. (1969) Phytochrome control of nyctinasty in Samanea as modified by oxygen, submergence, and chemicals. Plant Physiol. 22, 776–786Google Scholar
  35. Zeiger, E. (1983) The biology of stomatal guard cells. Annu. Rev. Plant Physiol. 34, 441–475Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • Cara Zucker Lowen
    • 1
  • Ruth L. Satter
    • 1
  1. 1.Department of Molecular and Cell BiologyUniversity of ConnecticutStorrsUSA

Personalised recommendations