Abstract
The electrical response to the synthetic auxin 1-naphthaleneacetic acid (1-NAA) of Nicotiana plumbaginifolia wild type and the monogenic, dominant auxinresistant mutant R25 was studied. Membrane potentials were continuously recorded in hypocotyl cells of light-grown, intact seedlings, and the time course of the response to 1-NAA addition was followed. Wild-type cells responded to ⩾ 10−5 M 1-NAA with a delayed, transient hyperpolarization. The R25 cells hyperpolarized significantly only in response to 1-NAA at 10−3 M, and with maximal amplitudes lower than those recorded with the wild type. In contrast, the two genotypes reacted similarly in terms of kinetics and amplitude to 10−5 M fusicoccin, which rapidly and strongly hyperpolarized the cells, and to 10−3 M benzoic acid, which induced rapid and weak hyperpolarization. The resting membrane potentials of the wild type and R25 were also not significantly different. Unlike wild-type hypocotyls, those of R25 ceased elongating before the time chosen for the electrophysiological measurements, but control experiments performed at a time when the elongation of both genotypes had terminated indicated that the difference in electrical response to auxin is independent of hypocotyl growth. The inefficiency of 1-NAA in inducing hyperpolarization of R25 hypocotyl cells suggests a defect at an early step in auxin action.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- 1-NAA:
-
1-naphthaleneacetic acid
References
Barbier-Brygoo, H., Ephritikhine, G., Klämbt, D., Maurel, C., Palme, K., Schell, J., Guern, J. (1991) Perception of the auxin signal at the plasma membrane of tobacco mesophyll protoplasts. Plant J. 1, 83–93
Bates, G.W., Goldsmith, M.H.M. (1983) Rapid responses of the plasmamembrane potential in oat coleoptiles to auxin and other weak acids. Planta 159, 231–237
Blatt, M.R. (1988) Mechanisms of fusicoccin action: a dominant role for secondary transport in a higher-plant cell. Planta 174, 187–200
Blatt, M.R., Thiel, G. (1994) K+ channels of stomatal guard cells: bimodal control of the K+ inward-rectifier evoked by auxin. Plant J. 5, 55–68
Blonstein, A.D., Stirnberg, P., King, P.J. (1991) Mutants of Nicotiana plumbaginifolia with specific resistance to auxin. Mol. Gen. Genet. 228, 361–371
Brummer, B., Felle, H., Parish, R.W. (1984) Evidence that acid solutions induce plant cell elongation by acidifying the cytosol and stimulating the proton pump. FEBS Lett. 174, 223–227
Cleland, R.E. (1982) The mechanism of auxin-induced proton efflux. In: Plant growth substances 1982, pp. 23–31, Wareing, P.F., ed. Academic Press, London New York
Cleland, R.E. (1990) Proton export, ATPase and hormone action. In: Molecular aspects of hormonal regulation of plant development, pp. 185–194. Kutáček, M., Elliott, M.C., Macháěková, I., eds. SPB Academic Publishing bv, The Hague
Cleland, R.E., Prins, H.B.A., Harper, J.R., Higinbotham, N. (1977) Rapid hormone-induced hyperpolarization of the oat coleoptile transmembrane potential. Plant Physiol. 59, 395–397
De Boer, A.H., Katou, K., Mizuno, A., Kojima, H., Okamoto, H. (1985) The role of electrogenic xylem pumps in K+ absorption from the xylem of Vigna unguiculata: the effects of auxin and fusicoccin. Plant Cell Environ. 8, 579–586
Ephritikhine, G., Barbier-Brygoo, H., Muller, J.-F., Guern, J. (1987) Auxin effect on the transmembrane potential difference of wild-type and mutant tobacco protoplasts exhibiting a differential sensitivity to auxin. Plant Physiol. 83, 801–804
Estelle, M. (1992) The plant hormone auxin: insight in sight. Bio Essays 14, 439–444
Evans, M.L. (1974) Rapid responses to plant hormones. Annu. Rev. Plant Physiol. 25, 195–223
Felle, H., Brummer, B., Bertl, A., Parish, R.W. (1986) Indole-3-acetic acid and fusicoccin cause cytosolic acidification of corn coleoptile cells. Proc. Natl. Acad. Sci. USA 83, 8992–8995
Felle, H., Peters, W., Palme, K. (1991) The electrical response of maize to auxins. Biochim. Biophys. Acta 1064, 199–204
Frachisse, J.-M., Johannes, E., Felle, H. (1988) The use of weak acids as physiological tools: a study of the effects of fatty acids on intracellular pH and electrical plasmalemma properties of Riccia fluitans rhizoid cells. Biochim. Biophys. Acta 938, 199–210
Guilfoyle, T.J. (1986) Auxin-regulated gene expression in higher plants. Crit. Rev. Plant Sci. 4, 247–276
Hayashi, H., Czaja, I., Lubenow, H., Schell, J., Walden, R. (1992) Activation of a plant gene by T-DNA tagging: auxin-independent growth in vitro. Science 258, 1350–1353
Ikoma, S., Okamoto, H. (1988) The quantitative and chronological relationship between IAA-induced H+-pump activation and elongation growth studied by means of xylem perfusion. Plant Cell Physiol. 29, 261–267
Katou, K. (1978) Distribution of electric potential and ion transport in the hypocotyl of Vigna sesquipedalis V. Electrogenic activity of the parenchyma cells in hypocotyl segments. Plant Cell Physiol. 19, 523–535
Leyser, H.M.O., Lincoln, C.A., Timpte, C., Lammer, D., Turner, J., Estelle, M. (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364, 161–164
Lohse, G., Hedrich, R. (1992) Characterization of the plasma-membrane H+-ATPase from Vicia faba guard cells. Planta 188, 206–214
Marré, E., Lado, P., Ferroni, A., Ballarin Denti, A. (1974) Transmembrane potential increase induced by auxin, benzyladenine and fusicoccin. Correlation with proton extrusion and cell enlargement. Plant Sci. Lett. 2, 257–265
Martinez-Cortina, C., Ullrich, C.I., Sanz, A. (1992) Hormone effects on the membrane potential and on sucrose-induced depolarization of young Citrus leaves. Plant Cell Physiol. 33, 1165–1170
Nelles, A. (1977) Short-term effects of plant hormones on membrane potential and membrane permeability of dwarf maize coleoptile cells (Zea mays L. d1 in comparison with growth responses). Planta 137, 293–298
Rayle, D.L., Cleland, R.E. (1992) The acid growth theory of auxin induced cell elongation is alive and well. Plant Physiol. 99, 1271–1274
Rück, A., Palme, K., Venis, M.A., Napier, R.M., Felle, H.H. (1993) Patchclamp analysis establishes a role for an auxin binding protein in the auxin stimulation of plasma membrane current in Zea mays protoplasts. Plant J. 4, 41–46
Sanders, D., Hansen, U.-P., Slayman, C.L. (1981) Role of the plasma membrane proton pump in pH regulation in non-animal cells. Proc. Natl. Acad. Sci. USA 78, 5903–5907
Senn, A.P., Goldsmith, M.H.M. (1988) Regulation of electrogenic proton pumping by auxin and fusicoccin as related to the growth of Avena coleoptiles. Plant Physiol. 88, 131–138
Spanswick, R.M. (1972) Electrical coupling between cells of higher plants: a direct demonstration of intercellular communication. Planta 102, 215–227
Stirnberg, P. (1994) Isolation and characterization of auxin-resistant mutants of Nicotiana plumbaginifolia. Ph.D. thesis, University of Basel, Switzerland
Author information
Authors and Affiliations
Additional information
The authors are grateful to Prof. Jean Guern and Dr. Michael Schultze (ISV, CNRS) for helpful discussions and critically reading the manuscript, and to Philippe Muller (ISV, CNRS) for computer scanning of the membrane-potential recordings. Fusicoccin was kindly provided by Dr. A. Ballio, University of Rome, Italy.
Rights and permissions
About this article
Cite this article
Stirnberg, P., King, P.J. & Barbier-Brygoo, H. An auxin-resistant mutant of Nicotiana plumbaginifolia Viv. is impaired in 1-naphthaleneacetic acid-induced hyperpolarization of hypocotyl cell membranes in intact seedlings. Planta 196, 706–711 (1995). https://doi.org/10.1007/BF00197335
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00197335