Skip to main content
Log in

Gravity-dependent polarity of cytoplasmic streaming inNitellopsis

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

The internodal cells of the characean algaNitellopsis obtusa were chosen to investigate the effect of gravity on cytoplasmic streaming. Horizontal cells exhibit streaming with equal velocities in both directions, whereas in vertically oriented cells, the downwardstreaming cytoplasm flows ca. 10% faster than the upward-streaming cytoplasm. These results are independent of the orientation of the morphological top and bottom of the cell. We define the ratio of the velocity of the downward- to the upward-streaming cytoplasm as the polar ratio (PR). The normal polarity of a cell can be reversed (PR<1) by treatment with neutral red (NR). The NR effect may be the result of membrane hyperpolarization, caused by the opening of K+ channels. The K+ channel blocker TEA Cl inhibits the NR effect.

External Ca2+ is required for normal graviresponsivness. The [Ca2+] of the medium determines the polarity of cytoplasmic streaming. Less than 1 μM Ca2+ resulted in a PR<1 while greater than 1 μM Ca2+ resulted in the normal gravity response. The voltage-dependent Ca2+ -channel blocker, nifedipine, inhibited the gravity response in a reversible manner, while treatment with LaCl3 resulted in a PR<1, indicating the presence of two types of Ca2+ channels. A new model for graviperception is presented in which the whole cell acts as the gravity sensor, and the plasma membrane acts as the gravireceptor. This is supported by ligation and UV irradiation experiments which indicate that the membranes at both ends of the cell are required for graviperception. The density of the external medium also affects the PR ofNitellopsis. Calculations are presented that indicate that the weight of the protoplasm may provide enough potential energy to open ion channels.

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

  • Audus LJ (1971) Linkage between detection and the mechanisms establishing differential growth factor concentration. In: Gordon SA, Cohen MJ (eds) Gravity and the organism. University of Chicago Press, Chicago, pp 137–150

    Google Scholar 

  • — (1979) Plant geosensors. J Exp Bot 30: 1051–1073

    Google Scholar 

  • Björkman T, Leopold AC (1987) Effect of inhibitors of auxin transport and of calmodulin on a gravisensing-dependent current in maize roots. Plant Physiol 84: 847–850

    Google Scholar 

  • Bottelier HP (1934) Über den Einfluß äußerer Faktoren auf die Protoplasmaströmung in derAvena-Koleoptile. Rec Trav Bot Néerl 31: 474–582

    Google Scholar 

  • Casper T, Pickard BG (1989) Gravitropism in a starchless mutant ofArabidopsis. Planta 177: 185–197

    Google Scholar 

  • Czapek F (1898) Weitere Beiträge zur Kenntniss der geotropischen Reizbewegungen. Jahrb Wiss Botanik 32: 12–308

    Google Scholar 

  • Dennison DS, Shropshire Jr W (1984) The gravireceptor ofPhycomyces. Its development following gravity exposure. J Gen Physiol 84: 845–859

    Google Scholar 

  • Ding D-Q, Tazawa M (1989) Influence of cytoplasmic streaming and turgor pressure gradient on the transnodal transport of rubidium and electrical conductance inChara corallina. Plant Cell Physiol 30: 739–748

    Google Scholar 

  • Dörr F (1983) Size and shape. In: Hoppe W, Lohmann W, Markl H, Zeigler H (eds) Biophysics. Springer, Berlin Heidelberg New York Tokyo, pp 42–50

    Google Scholar 

  • Edwards KL, Pickard BG (1987) Detections and transduction of physical stimuli in plants. In: Wagner E, Greppin H, Millet B (eds) The cell surface in signal transduction. Springer, Berlin Heidelberg New York Tokyo, pp 41–66

    Google Scholar 

  • Ewart AJ (1903) On the physics and physiology of protoplasmic streaming in plants. Clarendon Press, Oxford, 131 pp

    Google Scholar 

  • Grolig F, Wagner G (1989) Characterization of the isolated calciumbinding vesicles from the green algaMougeotia scalaris, and their relevance to chloroplast movement. Planta 177: 169–177

    Google Scholar 

  • Haberlandt G (1914) Physiological plant anatomy. Macmillian, London

    Google Scholar 

  • Hayashi T (1957) Some dynamic properties of the protoplasmic streaming inChara. Bot Mag (Tokyo) 70: 168–174

    Google Scholar 

  • Hejnowicz Z, Buchen B, Sievers A (1985) The endogenous difference in the rates of acropetal and basipetal cytoplasmic streaming inChara rhizoids is enhanced by gravity. Protoplasma 125: 219–230

    Google Scholar 

  • Howard J, Roberts WM, Hudspeth AJ (1988) Mechanoelectrical transduction by hair cells. Annu Rev Biophys Chem 17: 99–124

    Google Scholar 

  • Kamitsubo E (1972) Motile protoplasmic fibrils in cells of the characeae. Protoplasma 74: 53–70

    Google Scholar 

  • —, Kikuyama M, Kaneda I (1988) Apparent viscosity of the endoplasm of characean internodal cells measured by the centrifuge method. Protoplasma [Suppl 1]: 10–14

    Google Scholar 

  • —, Ohashi Y, Kikuyama M (1989) Cytoplasmic streaming in internodal cells ofNitella under centrifugal acceleration: a study done with a newly constructed centrifuge microscope. Protoplasma 152: 148–155

    Google Scholar 

  • Kamiya N, Kuroda K (1956) Artificial modification of the osmotic pressure of the plant cell. Protoplasma 46: 423–436

    Google Scholar 

  • — — (1957) Cell operation inNitella III. Specific gravity of the cell sap and endoplasm. Proc Jpn Acad Sci 33: 403–406

    Google Scholar 

  • — — (1958) Measurement of the motive force of the protoplasmic rotation inNitella. Protoplasma 50: 144–148

    Google Scholar 

  • Kamiya R, Witman GB (1984) Submicromolar levels of calcium control the balance of beating between the two flagella in demembranated models ofChlamydomonas. J Cell Biol 98: 97–107

    Google Scholar 

  • Kawamura G, Tazawa M (1980) Rapid light-induced potential change inChara cells stained with neutral red in the absence of internal Mg-ATP. Plant Cell Physiol 21: 547–559

    Google Scholar 

  • Kessler JO (1979) Gravity sensing, polar transport and cytoplasmic streaming in plant cells. Physiologist [Suppl] 22: S 47-S 48

    Google Scholar 

  • Kiss JZ, Hertel R, Sack FD (1989) Amyloplasts are necessary for full gravitropic sensitivity in roots ofArabidopsis thaliana. Planta 177: 198–206

    Google Scholar 

  • Lee JS, Mulkey TJ, Evans ML (1983 a) Gravity-induced polar transport of calcium across root tips of maize. Plant Physiol 73: 874–876

    Google Scholar 

  • — — — (1983 b) Reversible loss of gravitropic sensitivity in maize roots after tip application of calcium chelators. Science 220: 1375–1376

    Google Scholar 

  • Luby-Phelps K, Lanni F, Taylor DL (1988) The submicroscopic properties of cytoplasm as a determinant of cellular function. Annu Rev Biophys Biophys Chem 17: 369–396

    Google Scholar 

  • Lucas WJ, Shimmen T (1981) Intracellular perfusion and cell centrifugation studies on plasmalemma transport processes inChara corallina. J Membrane Biol 58: 227–237

    Google Scholar 

  • MacRobbie EAC, Banfield J (1988) Calcium influx at the plasmalemma ofChara corallina. Planta 176: 98–108

    Google Scholar 

  • McClure BA, Guilfoyle TJ (1989) Rapid redistribution of auxinregulated RNAs during gravitropism. Science 243: 91–93

    Google Scholar 

  • Moore R (1985 a) A morphometric analysis of the redistribution of organelles in columella cells in primary roots of normal seedlings and a gravitropic mutants ofHordeum vulgare. J Exp Bot 36: 1275–1286

    Google Scholar 

  • — (1985 b) Calcium movement, graviresponsiveness and the structure of columella cells and columella tissues in roots ofAllium cepa L. Ann Bot 56: 173–187

    Google Scholar 

  • — (1985 c) Movement of calcium across tips of primary and lateral roots ofPhaseolus vulgaris. Amer J Bot 72: 785–787

    Google Scholar 

  • —, Pasieniuk J (1984) Structure of columella cells in primary and lateral roots ofRicinus communis (Euphorbiaceae). Ann Bot 53: 715–726

    Google Scholar 

  • Olesen S-P, Clapman DE, Davies PF (1988) Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature 331: 168–170

    Google Scholar 

  • Perdue DO, LaFavre AK, Leopold AC (1988) Calcium in the regulation of gravitropism by light. Plant Physiol 86: 1276–1280

    Google Scholar 

  • Pickard BG, Thimann KV (1966) Geotropic response of wheat coleoptiles in absence of amyloplast starch. J Gen Physiol 49: 1065–1086

    Google Scholar 

  • Ransom JS, Moore R (1984) Geoperception in primary and lateral roots ofPhaseolus vulgaris (Fabaceae). II. Intracellular distribution of organelles in columella cells. Can J Bot 62: 1090–1094

    Google Scholar 

  • Roberts WM, Howard J, Hudspeth AJ (1988) Hair cells: transduction, tuning, and transmission in the inner ear. Annu Rev Cell Biol 4: 63–92

    Google Scholar 

  • Russ U, Grolig F, Wagner G (1988) Differentially adsorbed vital dyes inhibit chloroplast movement inMougeotia scalaris. Protoplasma [Suppl 1]: 180–184

    Google Scholar 

  • Sato T (1962) Effect of potassium, calcium, and magnesium ions on the protoplasmic streaming inAcetabularia calyculus. Bot Mag (Tokyo) 74: 384–390

    Google Scholar 

  • Shiina T, Tazawa M (1987 a) Ca2+ -activated Cl channel in plasmalemma ofNitellopsis obtusa. J Membrane Biol 99: 137–146

    Google Scholar 

  • — — (1987 b) Demonstration and characterization of Ca2+ channel in tonoplast-free cells ofNitellopsis obtusa. J Membrane Biol 96: 263–276

    Google Scholar 

  • — — (1988) Ca2+ -dependent Cl efflux in tonoplast-free cells ofNitellopsis obtusa. J Membrane Biol 106: 135–139

    Google Scholar 

  • Sievers A, Volkmann D (1979) Gravitropism in single cells. In: Haupt W, Feinleib ME (eds) Physiology of movements. Springer, Brlin Heidelberg New York, pp 567–572 [Pirson A, Zimmermann MH (eds) Encyclopedia of plant physiology, new series, vol 7]

    Google Scholar 

  • Slocum RD, Roux SJ (1983) Cellular and subcellular localization of calcium in gravistimulated oat coleoptiles and its possible significance in the establishment of tropic curvature. Planta 157: 481–492

    Google Scholar 

  • Tazawa M, Shimmen T (1980) Demonstration of the K+ channel in the plasmalemma of tonoplast-free cells ofChara australis. Plant Cell Physiol 21: 1535–1540

    Google Scholar 

  • Tominaga Y, Shimmen T, Tazawa M (1983) Control of cytoplasmic streaming by extracellular Ca2+ in permeabilizedNitella cells. Protoplasma 116: 75–77

    Google Scholar 

  • Tominaga Y, Muto S, Shimmen T, Tazawa M (1985) Calmodulin and Ca2+ -controlled cytoplasmic streaming in characean cells. Cell Struct Funct 10: 315–325

    Google Scholar 

  • Tsien RW, Hess P, McCleskey EW, Rosenberg RL (1987) Calcium channels: mechanisms of selectivity, permeation and block. Annu Rev Biophys Biophys Chem 16: 265–290

    Google Scholar 

  • Tsutsui I, Ohkawa T, Nagai R, Kishimoto U (1987) Role of calcium ion in the excitability and electrogenic pump activity of theChara corallina membrane: II. Effects of La3+, EGTA, and calmodulin antagonists on the current-voltage relation. J Membrane Biol 96: 75–84

    Google Scholar 

  • Vogel S (1983) Life in moving fluids. The physical biology of flow. Princeton University Press, Princeton

    Google Scholar 

  • Wayne R (1985) The contribution of calcium ions and hydrogen ions to the signal transduction chain in phytochrome-mediated fern spore germination. PhD Thesis, University of Massachusetts

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wayne, R., Staves, M.P. & Leopold, A.C. Gravity-dependent polarity of cytoplasmic streaming inNitellopsis . Protoplasma 155, 43–57 (1990). https://doi.org/10.1007/BF01322614

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01322614

Keywords

Navigation