Skip to main content
SpringerLink
Log in

Influence of calcium on blue-light-induced chloroplast movement in Lemna trisulca L.

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The presence of calcium is essential for chloroplast movement induced by blue light in Lemna trisulca L. The regulatory role of calcium was confirmed by the inhibition of chloroplast movement by cytochalasin B and trifluoperazine. The calcium concentration in tissues was modified by ethylene glycol-bis(2-aminoethylether)-N,N,N′, N′-tetraacetic acid (EGTA), the calcium ionophore A23187 and La3+. Only a long period of incubation (12h) in EGTA or La3+ caused distrubances in chloroplast movement. This indicates that calcium influx is not essential for chloroplast movement. Those conditions that dramatically changed the internal calcium concentration, either applications of calcium ionophore A23187 and EGTA, or ionophore and La3+, markedly decreased the amplitude of response to blue-light pulses. This demonstrates that disturbances of chloroplast movement are observable only when internal stores of calcium are affected by Ca2+-antagonists. We suggest that the calcium involved in blue-light-induced chloroplast movement is derived from intracellular stores. The addition of Mg2+ to EGTA buffer counteracted its effect, indicating that Mg2+, as well as Ca2+, might possibly be involved in chloroplast movement.

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

Access this article

Log in via an institution

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

EGTA:

ethylene glycol-bis(2-aminoethylether)-N,N,N′,N′-tetraacetic acid

Hepes:

4(2-hydroxyethyl-1-piperazine) ethanesulfonic acid

A23187:

calcium ionophore

References

  • Äkerman, K.E.O., Proudlove, M.O., Moore, A.L. (1983) Evidence for a Ca2+ gradient across the plasma membrane of wheat protoplasts. Biochem. Biophys. Res. Commun. 113, 171–177

    Google Scholar 

  • Amellal, M., Landry, Y. (1983) Lanthanides are transported by ionophore A 23187 and mimic calcium in the histamine secretion process. Br. J. Pharmac. 80, 365–370

    Google Scholar 

  • Bonner, J., Galston, A.W. (1952) Principles of plant physiology. Freeman, San Francisco

    Google Scholar 

  • Calbiochem, Biochemical/Immunochemical Catalog (1989), pp. 216–222

  • Campbell, A.K. (1983) Intracellular calcium. John Wiley & Sons, Inc., New York

    Google Scholar 

  • Campbell, A.K., Siddle, K. (1976) The effect of intracellular calcium ions on adrenaline-stimulated adenosine 3′: 5′-cyclic monophosphate concentrations in pigeon erythrocytes: studies by using ionophore A 23187. Biochem. J. 158, 211–221

    Google Scholar 

  • Campbell, A.K., Thomson, W.W. (1977) Effects of lanthanum and ethylenediaminetetraacetate on leaf movements of Mimosa. Plant Physiol. 60, 635–639

    Google Scholar 

  • Chlobowski, A. (1986) Photometric method in chloroplast movement investigation. Photosynthetica 20, 486–493

    Google Scholar 

  • Dreyer, E.M., Weisenseel, M.H. (1979) Phytochrome-mediated uptake of calcium in Mougeotia cells. Planta 146, 31–39

    Google Scholar 

  • Gabryś, H., Walczak, T. (1980) Photometric study of chloroplast phototranslocations in leaves of land plants. Physiol. Plant. II, 281–290

    Google Scholar 

  • Galland, P., Senger, H. (1988) The role of flavins as photoreceptors. J. Photochem. Photobiol. 1, 277–294

    Google Scholar 

  • Gilroy, S., Hughes, W.A., Trewavas, A.J. (1989) A comparison between Quin-2 and aequorin as indicators of cytoplasmic calcium levels in higher plant cell protoplasts. Plant Physiol. 90, 482–491

    Google Scholar 

  • Gilroy, S., Fricker, M.D., Read, N.D., Trewavas, A.J. (1991) Role of calcium in signal transduction of Commelina guard cells. Plant Cell. 3, 333–344

    Google Scholar 

  • Grolig, F., Wagner, G. (1987) Vital staining permits isolation of the calcium vesicles from the green alga Mougeotia. Planta 171, 433–437

    Google Scholar 

  • Grolig, F., Wagner, G. (1988) Light-dependent chloroplast rerientations in Mougeotia and Mesotaenium: biased by pigment-regulated plasmalemma anchorage sites to actin filaments? Bot. Acta 101, 2–6

    Google Scholar 

  • Grolig, F., Wagner, G. (1989) Characterization of the isolated calcium-binding vesicles from the green alga Mougeotia scalaris, and their relevance to chloroplast movement. Planta 177, 169–177

    Google Scholar 

  • Hart, J.W., Sabnis, D.D. (1976) Colchicine and plant microtubules: A critical evaluation. Curr. Adv. Plant. Sci. 8, 1095–1104

    Google Scholar 

  • Haupt, W. (1959) Die Chloroplastendrehung bei Mougeotia. I. Über den quantitativen und qualitativen Lichtbedarf der Schwachlichtbewegung. Planta 53, 484–501

    Google Scholar 

  • Haupt, W. (1983) Movement of chloroplasts under the control of light. Prog. Physiol. Res. 2, 227–281

    Google Scholar 

  • Haupt, W., Scheuerlein, R. (1990) Chloroplast movement. Plant Cell Environ. 13, 595–614

    Google Scholar 

  • Haupt, W., Wagner, G. (1984) Chloroplast movement. In: Membranes and sensory transduction, pp. 331–3375, Colombetti, G., Lenci, F., eds. Plenum, New York

    Google Scholar 

  • Haupt, W., Weisenseel, M.H. (1976) Physiological evidence and some thoughts on localized responses, intracellular localization and action of phytochrome. In: Light and plant development, pp. 63–74, Smith, H., ed. Butterworths, Boston

    Google Scholar 

  • Hepler, P., Palevitz, B. (1974) Microtubules and microfilaments. Annu. Rev. Plant Physiol. 25, 309–362

    Google Scholar 

  • Herth, W. (1978) Ionophore A 23187 stops tip growth, but not cytoplasmic streaming, in pollen tubes of Lilium longiflorum. Protoplasma 96, 275–282

    Google Scholar 

  • Inagaki, M., Tanaka, T., Sasaki, Y., Hidaka, H. (1985) Calcium dependent interactions of an ionophore A 23187 with calmodulin. Biochem. Biophys. Res. Commun. 130, 200–206

    Google Scholar 

  • Jacobshagen, S., Altmüller, D., Grolig, F., Wagner, G. (1986) Calcium pools, calmodulin and light-regulated chloroplast movements in Mougeotia and Mesotaenium. In: Molecular and cellular aspects of calcium in plant development, pp. 201–209, Trewavas, A.J., ed. Plenum, New York

    Google Scholar 

  • Lettvin, J.Y., Pickard, W.F., McCulloch, W.S., Pitts, W. (1964) A theory of passive ion flux through axon membranes. Nature 202, 1338–1339

    Google Scholar 

  • Lew, R.R., Serlin, B.S., Schauf, C.L., Stockton, M.E. (1990) Calcium activation of Mougeotia potassium channels. Plant Physiol. 92, 831–836

    Google Scholar 

  • Lynch, T.J. (1979) Human erythrocyte Ca2+-Mg2+-ATPase: mechanism of stimulation by Ca2+. Arch. Biochem. Biophys. 194, 165–179

    Google Scholar 

  • Pfeiffer, D.R., Reed, P.W., Lardy, H.A. (1974) Ultraviolet and fluorescent spectral properties of the divalent cation ionophore A 23187 and its metal ion complexes. Biochemistry 13, 4007–4014

    Google Scholar 

  • Reid, R.J., Smith, F.A. (1992) Measurement of calcium fluxes in plants using 45Ca. Planta 186, 558–556

    Google Scholar 

  • Russ, U., Grolig, F., Wagner, G. (1991) Changes of cytoplasmic free Ca2+ in the green alga Mougeotia scalaris as monitored with indo-1, and their effect on the velocity of chloroplast movements. Planta 184, 105–112

    Google Scholar 

  • Schönbohm, E., Meyer-Wegener, J., Schönbohm, E. (1990) No evidence for influx as an essential link in the signal transduction chains of either light-oriented chloroplast movements or Pfr-mediated chloroplast anchorage in Mougeotia. J. Photochem. Photobiol. 5, 331–341

    Google Scholar 

  • Serlin, B.S., Ferrel, S. (1991) The involvement of microtubules in chloroplast rotation in the alga Mougeotia. Plant Sci. 60, 1–8

    Google Scholar 

  • Serlin, B.S., Roux, S.J. (1984) Modulation of chloroplast movement in the green alga Mougeotia by the Ca2+ ionophore A 23187 and by calmodulin antagonists. Proc. Natl. Acad. Sci. USA 81, 6368–6372

    Google Scholar 

  • Thomson, W.W., Platt, K.A., Campbell, N. (1973) The use of lanthanum to delineate the apoplastic continuum in plants. Cytobios 8, 57–62

    Google Scholar 

  • Tretyn, A., Kendrick, R.E., Wagner, G. (1991) The role(s) of calcium ions in phytochrome action. Photochem. Photobiol. 54, 1135–1155

    Google Scholar 

  • Wagner, G., Bellini, E. (1976) Light-dependent fluxes and compartmentation of calcium in the green alga Mougeotia. Z. Pflanzenphysiol. 79, 283–291

    Google Scholar 

  • Wagner, G., Klein, K. (1978) Differential effects of calcium on chloroplast movement in Mougeotia. Photochem. Photobiol. 27, 137–140

    Google Scholar 

  • Wagner, G., Klein, K. (1981) Mechanism of chloroplast movement in Mougeotia. Protoplasma 109, 169–185

    Google Scholar 

  • Wagner, G., Rossbacher, R. (1980) X-ray microanalysis and chlorotetracycline staining of calcium vesicles in the green alga Mougeotia. Planta 149, 298–305

    Google Scholar 

  • Wagner, G., Grolig, F. (1985) Molecular mechanisms of photoinduced chloroplast movement. In: Sensory perception and transduction in aneural organisms, pp. 281–298, Colombetti, G., Lenci, F., Song, P.S., eds. Plenum Press, New York

    Google Scholar 

  • Wagner, G., Grolig, F., Altmüller, D. (1987) Transduction chain of low irradiance response of chloroplast reorientation in Mougeotia in blue or red light. Photochem. Photobiophys. Suppl. 183–189

  • Wagner, G., Valentin, P., Dieter, P., Marmé, D. (1984) Identification of calmodulin in the green alga Mougeotia and its possible function in chloroplast reorientational movement. Planta 162, 62–67

    Google Scholar 

  • Walczak, T., Gabryś, H. (1980) New type of photometer for measurements of transmission changes corresponding to chloroplast movements in leaves. Photosynthetica 14, 65–72

    Google Scholar 

  • Wayne, R., Hepleŕ, P.K. (1984) The role of calcium ions in phytochrome germination of Onoclea sensibilis L. Planta 160, 12–20

    Google Scholar 

  • Wayne, R., Hepler, P.K. (1985) Red light stimulates an increase in intracellular calcium in the spores of Onoclea sensibilis. Plant Physiol. 77, 8–11

    Google Scholar 

  • Weidinger, M., Ruppel, H.G. (1985) Ca2+-requirement for a bluelight-induced chloroplast translocation in Eremosphaera viridis. Protoplasma 124, 184–187

    Google Scholar 

  • Weiss, G.B. (1974) Cellular pharmacology of lanthanum. Annu. Rev. Pharmacol. 14, 343–354

    Google Scholar 

  • Zurzycki, J. (1962) The actin spectrum for the light dependent movements of chloroplasts in Lemna trisulca L. Acta Soc. Bot. Polon. 31, 489–538

    Google Scholar 

  • Zurzycki, J. (1972) Primary reactions in the chloroplast rearrangements. Acta Protozool. 11, 189–200

    Google Scholar 

  • Zurzycki, J. (1980) Blue-light-induced intracellular movements. In: The blue light syndrome, pp. 50–68, Senger, H., ed. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Zurzycki, J., Walczak, T., Gabryś, H., Kajfosz, J. (1983) Chloroplast translocations in Lemna trisulca L. induced by continuous irradiation and by light pulses. Kinetics analysis. Planta 157, 502–510

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry and Physics, Academy of Agriculture, Al. Mickiewicza 24/28, PL-30-059, Krakow, Poland

    Monika Tlałka

  2. Institute of Molecular Biology, Jagiellonian University, Al. Mickiewicza 3, PL-31-120, Krakow, Poland

    Halina Gabryś

Authors
  1. Monika Tlałka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Halina Gabryś
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

We express our gratitude to Professor W. Korohoda for valuable critical comments on this paper and stimulating discussion. We also thank Mr. P. Malec for help in preparing the experiment with trifluoperazine and Mr. A. Waloszek for taking the photographs. We are indebted to Mr. Tim Kline (International House, Krakow, Poland) for improving the English style. This research was supported by grant No. 1042/P2/92/03 from the State Committe for Scientific Research.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tlałka, M., Gabryś, H. Influence of calcium on blue-light-induced chloroplast movement in Lemna trisulca L.. Planta 189, 491–498 (1993). https://doi.org/10.1007/BF00198211

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00198211

Key words

Search

Navigation