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.
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
— (1979) Plant geosensors. J Exp Bot 30: 1051–1073
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
Bottelier HP (1934) Über den Einfluß äußerer Faktoren auf die Protoplasmaströmung in derAvena-Koleoptile. Rec Trav Bot Néerl 31: 474–582
Casper T, Pickard BG (1989) Gravitropism in a starchless mutant ofArabidopsis. Planta 177: 185–197
Czapek F (1898) Weitere Beiträge zur Kenntniss der geotropischen Reizbewegungen. Jahrb Wiss Botanik 32: 12–308
Dennison DS, Shropshire Jr W (1984) The gravireceptor ofPhycomyces. Its development following gravity exposure. J Gen Physiol 84: 845–859
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
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
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
Ewart AJ (1903) On the physics and physiology of protoplasmic streaming in plants. Clarendon Press, Oxford, 131 pp
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
Haberlandt G (1914) Physiological plant anatomy. Macmillian, London
Hayashi T (1957) Some dynamic properties of the protoplasmic streaming inChara. Bot Mag (Tokyo) 70: 168–174
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
Howard J, Roberts WM, Hudspeth AJ (1988) Mechanoelectrical transduction by hair cells. Annu Rev Biophys Chem 17: 99–124
Kamitsubo E (1972) Motile protoplasmic fibrils in cells of the characeae. Protoplasma 74: 53–70
—, Kikuyama M, Kaneda I (1988) Apparent viscosity of the endoplasm of characean internodal cells measured by the centrifuge method. Protoplasma [Suppl 1]: 10–14
—, 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
Kamiya N, Kuroda K (1956) Artificial modification of the osmotic pressure of the plant cell. Protoplasma 46: 423–436
— — (1957) Cell operation inNitella III. Specific gravity of the cell sap and endoplasm. Proc Jpn Acad Sci 33: 403–406
— — (1958) Measurement of the motive force of the protoplasmic rotation inNitella. Protoplasma 50: 144–148
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
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
Kessler JO (1979) Gravity sensing, polar transport and cytoplasmic streaming in plant cells. Physiologist [Suppl] 22: S 47-S 48
Kiss JZ, Hertel R, Sack FD (1989) Amyloplasts are necessary for full gravitropic sensitivity in roots ofArabidopsis thaliana. Planta 177: 198–206
Lee JS, Mulkey TJ, Evans ML (1983 a) Gravity-induced polar transport of calcium across root tips of maize. Plant Physiol 73: 874–876
— — — (1983 b) Reversible loss of gravitropic sensitivity in maize roots after tip application of calcium chelators. Science 220: 1375–1376
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
Lucas WJ, Shimmen T (1981) Intracellular perfusion and cell centrifugation studies on plasmalemma transport processes inChara corallina. J Membrane Biol 58: 227–237
MacRobbie EAC, Banfield J (1988) Calcium influx at the plasmalemma ofChara corallina. Planta 176: 98–108
McClure BA, Guilfoyle TJ (1989) Rapid redistribution of auxinregulated RNAs during gravitropism. Science 243: 91–93
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
— (1985 b) Calcium movement, graviresponsiveness and the structure of columella cells and columella tissues in roots ofAllium cepa L. Ann Bot 56: 173–187
— (1985 c) Movement of calcium across tips of primary and lateral roots ofPhaseolus vulgaris. Amer J Bot 72: 785–787
—, Pasieniuk J (1984) Structure of columella cells in primary and lateral roots ofRicinus communis (Euphorbiaceae). Ann Bot 53: 715–726
Olesen S-P, Clapman DE, Davies PF (1988) Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature 331: 168–170
Perdue DO, LaFavre AK, Leopold AC (1988) Calcium in the regulation of gravitropism by light. Plant Physiol 86: 1276–1280
Pickard BG, Thimann KV (1966) Geotropic response of wheat coleoptiles in absence of amyloplast starch. J Gen Physiol 49: 1065–1086
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
Roberts WM, Howard J, Hudspeth AJ (1988) Hair cells: transduction, tuning, and transmission in the inner ear. Annu Rev Cell Biol 4: 63–92
Russ U, Grolig F, Wagner G (1988) Differentially adsorbed vital dyes inhibit chloroplast movement inMougeotia scalaris. Protoplasma [Suppl 1]: 180–184
Sato T (1962) Effect of potassium, calcium, and magnesium ions on the protoplasmic streaming inAcetabularia calyculus. Bot Mag (Tokyo) 74: 384–390
Shiina T, Tazawa M (1987 a) Ca2+ -activated Cl− channel in plasmalemma ofNitellopsis obtusa. J Membrane Biol 99: 137–146
— — (1987 b) Demonstration and characterization of Ca2+ channel in tonoplast-free cells ofNitellopsis obtusa. J Membrane Biol 96: 263–276
— — (1988) Ca2+ -dependent Cl− efflux in tonoplast-free cells ofNitellopsis obtusa. J Membrane Biol 106: 135–139
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]
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
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
Tominaga Y, Shimmen T, Tazawa M (1983) Control of cytoplasmic streaming by extracellular Ca2+ in permeabilizedNitella cells. Protoplasma 116: 75–77
Tominaga Y, Muto S, Shimmen T, Tazawa M (1985) Calmodulin and Ca2+ -controlled cytoplasmic streaming in characean cells. Cell Struct Funct 10: 315–325
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
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
Vogel S (1983) Life in moving fluids. The physical biology of flow. Princeton University Press, Princeton
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
Author information
Authors and Affiliations
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01322614