Abstract
Pattern formation mechanisms in developing organisms determine cellular differentiation and function. However, the components that interact during the manifestation of a spatial pattern are in general unknown. Characean algae represent a model system to study pattern formation. These algae develop alternating acid and alkaline transport domains that influence the pattern of growth. In the present study, it will be demonstrated that a diffusion mechanism is implicated in acid and alkaline domain formation and this growth pattern. Experiments on the characean growth pattern were performed that resulted in pronounced, however, unpredictable modifications in the original pattern. A major component involved in this pattern-forming mechanism emerged from the nonlinear kinetics of the H+-ATPase that is located in the plasma membrane of these algae. Based on these kinetics, a mathematical model was developed and numerically analyzed. As a result, the contribution of a diffusional component to the characean acid/alkaline pattern appeared most likely.
Similar content being viewed by others
References
Acton, F.S. 1970. Numerical Methods that Work. Harper and Row, New York.
Benjacob, E., Shmueli, H., Schochet, O., Tenebaum, A. 1992. Adaptive self-organization during growth of bacterial colonies. Physica A. 187:378–424
Carpita, N.C., Gibeaut, D.M. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with physical properties of the walls during growth. Plant J. 3:1–30
Fisahn, J., McConnaughey, T., Lucas, W.J. 1989. Oscillations in extracellular current, external pH and membrane potential and conductance in the alkaline bands of Nitella and Chara. J. Exp. Bot. 40:1185–1193
Fisahn, J., Lucas, W.J. 1990a. Inversion of extracellular current and axial voltage profile in Chara and Nitella. J. Membrane Biol. 113:1–8
Fisahn, J., Lucas, W.J. 1990b. Effects of microtubule-specific agents on the spatial and electrical properties of the plasma membrane in Chara comllina. Planta 182:506–512
Fisahn, J., Lucas, W.J. 1991. Autonomous local area control over membrane transport in Chara internodal cells. Plant Physiol. 95:1138–1143
Fisahn, J., Lucas, W.J. 1992. Direct measurement of the reversal potential and current-voltage characteristics in the acid and alkaline regions of Chara corallina. Planta 186:241–248
Fisahn, J., Hansen, U.P., Lucas, W.J. 1992. Reaction kinetic model of the Chara plasma-membrane 2 cycle H+-ATPase. Proc. Natl. Acad. Sci. USA 89:3261–3265
Gear, C.W. 1971. Numerical Initial Value Problems in Ordinary Differential Equations. Prentice Hall, Englewood Cliffs, NJ
Goodner, B., Quatrano, R. 1993. Fucus embryogenesis: a model to study the establishment of polarity. Plant Cell 5:1471–1481
Green, P.B. 1992. Pattern formation in shoots — a likely role for minimal energy configurations of the tunica. Int. J. Plant Sci. 153:59–75
Harrison, L.G. 1992. Reaction-diffusion theory and intracellular differentiation. Int. J. Plant Sci. 153:76–85
Jackson, J.D. 1993. Classical Electrodynamics. DeGruyter, Berlin
Jaffe, L.F. 1977. Electrophoresis along cell membranes. Nature 265:600–602
Jaffe, L.F. 1981. The role of ion currents in establishing developmental gradients In: International Cell Biology. H.G. Schweiger, editor. pp. 507–511
Jaffe, L.F., Nuccitelli, R. 1977. Electrical controls of development. Ann. Rev. Biophys. Bioeng. 6:445–476
Keller, H.B. 1968. Numerical Methods for Two-Point Boundary-Value Problems. Blaisdell, Waltham, MA
Levin, S.A., Segel, L.A. 1985. Pattern generation in space and aspect. SIAM Rev. 27:45–67
Lucas, W.J. 1982. Mechanism of acquisition of exogeneous bicarbonate by internodal cells of Chara corallina. Planta 156:181–192
Lucas, W.J. 1983. Photosynthetic assimilation of exogeneous HCO −3 by aquatic plants. Annu. Rev. Plant Physiol. 34:71–104
Lucas, W.J., Nuccitelli, R. 1890. HCO −3 and OH− transport across the plasmalemma of Chara: spatial resolution obtained using extracellular vibrating probe. Planta 150:120–131
Metraux, J.P., Richmond, P.A., Taiz, L. 1980. Control of cell elongation in Nitella by endogenous cell wall pH gradients. Multiaxial extensibility and growth studies. Plant Physiol. 65:204–210
Murray, J.D. 1989. Mathematical Biology. Springer-Verlag, Berlin
Nagorcka, B.N. 1986. The role of a reaction-diffusion system in the initiation of skin organ primordia. I. The first wave of initiation. J. Theor. Biol. 121:449–475
Nagorcka, B.N. 1988. A pattern formation mechanism to control spatial organization in the embryo of Drosophila melanogaster. J. Theor. Biol. 132:277–306
Nuccitelli, R. 1986. A two dimensional vibrating probe with a computerized graphics display. In: Ionic Currents in Development. R. Nuccitelli, editor, pp. 13–20. Alan R. Liss, New York
Press, W.H., Flannery, B.P., Teukolsky, S.A., Vetterling, W.T. 1990. Numerical Recipes in C. Cambridge University Press, Cambridge
Quatrano, R.S. 1978. Development of cell polarity. Ann. Rev. Plant Phys. 29:487–510
Quatrano, R.S. 1990. Polar axis fixation and cytoplasmic localization in Fucus. In: Genetics of Pattern Formation and Growth Control, pp. 31–46. Wiley-Liss, New York
Smith, F.A., Walker, N.A. 1976. Chloride transport in Chara corallina and the electrochemical potential difference for hydrogen ions. Exp. Bot. 27:451–459
Spanswick, R. 1981. Electrogenic ion pumps. Annu. Rev. Plant Physiol. 32:267–289
Spear, D.G., Barr, J.K., Barr, C.E. 1969. Localization of hydrogen ion and chloride fluxes in Nitella. J. Gen. Physiol. 54:397–414
Swindale, N.V. 1980. A model for the formation of ocular dominance stripes. Proc. Roy. Soc. Lond. B208:243–264
Turing, A.M. 1952. The chemical basis of morphogenesis. Phil. Trans. Roy. Soc. Lond. B237:37–72
Wagner, V.T., Brian, L., Quatrano, R.S. 1992. Role of a vitronectin-like molecule in embryo adhesion of the brown alga. Fucus. Proc. Natl. Acad. Sci. USA 89:3644–3648
Wolpert, L. 1969. Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25:1–47
Wolpert, L. 1971. Positional information and pattern formation. Curr. Top. Dev. Biol. 6:183–224
Wolpert, L. 1981. Positional information and pattern formation. Phil. Trans. Roy. Soc. Lond. B295:441–150
Author information
Authors and Affiliations
Additional information
This work was supported by the Deutsche Forschungsgemeinschaft (grant #571 1/1) to JF.
Rights and permissions
About this article
Cite this article
Fisahn, J., Lucas, W.J. Spatial organization of transport domains and subdomain formation in the plasma membrane of Chara corallina . J. Membarin Biol. 147, 275–281 (1995). https://doi.org/10.1007/BF00234525
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00234525