Abstract
I have investigated changes in electrical current across the plasma membrane that occur during cytokinin-induced bud formation in Funaria hygrometrica Hedw., using a non-intrusive vibrating microelectrode. Before cytokinin treatment the target caulonema cells have maximal inward current at the nuclear region. After cytokinin treatment inward current increases twofold along the length of the cell. Within minutes, however, current decreases at both the nuclear zone and the proximal end while increasing at the distal end of target cells, preceding and predicting the presumptive division site. Inward current at the distal end falls to resting levels after establishment of a bulging growth zone, and remains low around developing buds. This current is blocked by gadolinium nitrate, a Ca2+-uptake inhibitor, indicating a Ca2+ component of the current. The polarity of the target cells can be disrupted by microfilament inhibitors and cytokinin-induced buds form over the nucleus, halfway along the length of the cell. I suggest that cytokinin activates plasma-membrane ion channels which are subsequently redistributed to the distal ends of target cells by a microfilament-dependent process. Cytokinin-induced concentration of ion channels over presumptive bud sites may be envisioned to exert spatial control of cytoplasmic ion concentrations and stimulate bud formation by establishing a new growth zone, directing nuclear migration, and stimulating cell division.
Similar content being viewed by others
Abbreviations
- BA:
-
6-benzyladenine
- [Ca2+]i :
-
intracellular calcium-ion concentration
References
Bopp, M. (1982) How can external hormones regulate the morphogenesis of mosses? J. Hattori Bot. Lab. 53, 159–169
Brandes, H., Kende, H. (1968) Studies on cytokinin-controlled bud formation in moss protonemata. Plant Physiol. 43, 827–837
Brawley, S.H., Robinson, K.R. (1985) Cytochalasin treatment disrupts the endogenous currents associated with cell polarization in fucoid zygotes: Studies of the role of F-actin in embryogenesis. J. Cell Biol. 100, 1173–1184
Chen, T.-H., Jaffe, L.F. (1979) Forced calcium entry and polarized growth of Funaria spores. Planta 144, 401–406
Conrad, P.A., Hepler, P.K. (1984) Ultrastructural changes associated with cytokinin induced bud formation in the moss Funaria hygrometrica. (Abstr.) J. Cell Biol. 99, 244a
dos Remedios, C.G. (1981) Lanthanide ion probes of calcium-binding sites on cellular membranes. Cell Calcium 2, 29–51
Dustin, P. (1978) Microtubules. Springer, Berlin
Hepler, P.K. (1985) Calcium restriction prolongs metaphase in dividing Tradescantia stamen hair cells. J. Cell Biol. 100, 1363–1368
Herth, W. (1983) Taxol affects cytoskeletal microtubules, flagella and spindle structure of the crysoflagellate alga Poterioochromonas. Protoplasma 115, 228–239
Hesketh, T.R., Moore, J.P., Morris, J.D.H., Taylor, M.V., Roberts, J., Smith, G.A., Metcalfe, J.C. (1985) A common sequence of calcium and pH signals in the mitogenic stimulation of eukaryotic cells. Nature 313, 481–484
Jaffe, L.F. (1979) Control of development by ionic currents. In: Membrane transduction mechanisms, pp. 199–231, Cone, R.A., Dowling, J.E., eds. Raven Press, New York
Jaffe, L.F., Nuccitelli, R. (1974) An ultrasensitive vibrating electrode for measuring steady extracellular currents. J. Cell Biol. 63, 614–628
Jaffe, L.F., Robinson, K.R., Nuccitelli, R. (1974) Local cation entry and self electrophoresis as an intracellular localizing mechanism. Ann. N.Y. Acad. Sci. 238, 372–389
Jaffe, L.A., Weisenseel, M.H., Jaffe, L.F. (1975) Calcium accumulations within the growing tips of pollen tubes. J. Cell Biol. 67, 488–492
Kropf, D.L., Lupa, M.D.A., Caldwell, J.H., Harold, F.M. (1983) Cell polarity: endogenous ion currents precede and predict branching in the water mold Achlya. Science 220, 1385–1387
Kropf, D.L., Caldwell, J.H., Gow, N.A.R., Harold, F.M. (1984) Transcellular ion currents in the water mold Achlya. Amino acid proton symport as a mechanism of current entry. J. Cell Biol. 99, 486–496
Laetsch, W.M. (1967) Ferns. In: Methods in developmental biology, pp. 319–328, Wilt, F.H., Wessells, N.K., eds. Thomas Y. Crowell Co., New York
Letham, D.S. (1978) Cytokinins. In: Phytohormones and related compounds — a comprehensive treatise, vol. I: The biochemistry of phytohormones and related compounds, pp. 205–263, Letham, D.S., Goodwin, P.B., Higgins, T.J.V., eds. Elsevier, North Holland Biomedical Press, Amsterdam Oxford New York
Meindl, U. (1983) Cytoskeletal control of nuclear migration and anchoring in developing cells of Micrasterias denticulata and the change caused by the anti-microtubular herbicide amiprophos-methyl (AMP). Protoplasma 118, 75–90
Nuccitelli, R. (1978) Ooplasmic segregation and secretion in the Pelvetia egg is accompanied by a membrane-generated electrical current. Dev. Biol. 62, 13–33
Robinson, K.R., Jaffe, L.F. (1975) Polarized fucoid eggs drive a calcium current through themselves. Science 187, 70–72
Saunders, M.J., Helper, P.K. (1981) Localization of membrane-associated calcium following cytokinin treatment in Funaria using chlorotetracycline. Planta 152, 272–281
Saunders, M.J., Hepler, P.K. (1982) Ca2+ ionophore A23187 stimulates cytokinin-like mitosis in Funaria. Science 217, 943–945
Saunders, M.J., Hepler, P.K. (1983) Calcium antagonists and calmodulin inhibitors block cytokinin-induced bud formation in Funaria. Dev. Biol. 99, 41–49
Saunders, M.J. (1985) Plasma membrane ionic currents fluctuate during cytokinin-induced and normal cell division. Plant Physiol. 77, 21 a
Schatten, G., Schatten, H., Bestor, T.H., Balezon, R. (1982) Taxol inhibits the nuclear movements during fertilization and induces asters in unfertilized sea urchin eggs. J. Cell Biol. 94, 455–465
Schiff, P.B., Fant, J., Horwitz, S.B. (1979) Promotion of microtubule assembly in vitro by taxol. Nature 277, 665–667
Wani, M.C., Taylor, H.L., Wall, M.E., Coggin, P., McPhail, A.T. (1971) Plant antitumor agents. VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J. Am. Chem. Soc. 93, 2325–2327
Waaland, S.D., Lucas, W.J. (1984) An investigation of the role of transcellular ion currents in morphogenesis of Griffithsia pacifica Kylin. Protoplasma 123, 184–191
Weisenseel, M.H., Kicherer, R.M. (1981) Tonic currents as control mechanism in cytomorphogenesis. In: Cytomorphogenesis in plants, pp. 379–399, Kiermayer, O. ed. Springer, Wien New York
Weisenseel, M.H., Nuccitelli, R., Jaffe, L.F. (1975) Large electrical currents traverse growing pollen tubes. J. Cell Biol. 66, 556–567
Wessells, N.K., Spooner, B.S., Ash, J.F., Bradley, M.D., Luduena, M.A., Taylor, E.L., Wrenn, J.T., Yamada, K.M. (1971) Microfilaments in cellular and developmental processes. Science 171, 135–143
Williamson, R.E. (1984) Calcium and the plant cytoskeleton. Plant Cell Environ. 7, 432–440
Yin, H.L., Stossel, T.P. (1982) Calcium control of actin network structure by gelsolin. In: Calcium and cell function, vol. II, pp. 325–377, Cheung, W.Y., ed. Academic Press, New York London
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Saunders, M.J. Cytokinin activation and redistribution of plasma-membrane ion channels in Funaria . Planta 167, 402–409 (1986). https://doi.org/10.1007/BF00391346
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00391346