Abstract
The characteristics of transmembrane transport of 14C-labelled indol-3yl-acetic acid ([1-14C]IAA) were compared in Chlorella vulgaris Beij., a simple unicellular green alga, and in Chara vulgaris L., a branched, multicellular green alga exhibiting axial polarity and a high degree of cell and organ specialization. In Chara thallus cells, three distinguishable trans-plasmamembrane fluxes contributed to the net uptake of [1-14C]-IAA from an external solution, viz.: a non-mediated, pH-sensitive influx of undissociated IAA (IAAH); a saturable influx of IAA; and a saturable efflux of IAA. Both saturable fluxes were competitively inhibited by unlabelled IAA. Association of [3H]IAA with microsomal preparations from Chara thallus tissue was competitively inhibited by unlabelled IAA. Results indicated that up-take carriers occurred in the membranes at a much higher density than efflux carriers. The efflux component of IAA net uptake by Chara was not affected by several phytotropins (N-1-naphthylphthalmic acid, NPA; 2-(1-pyrenoyl)benzoic acid; and 5-(2-carboxyphenyl)-3-phenylpyrazole), which are potent non-competitive inhibitors of specific auxin-efflux carriers in more advanced plant groups, and no evidence was found for a specific association of [3H]NPA with Chara microsomal preparations. It was concluded that Chara lacked phytotropin receptors. Net uptake of [1-14C]IAA also was unaffected by 2,3,5-triiodobenzoic acid except at concentrations (≥ 10−1 mol · m−3) high enough to depress cytoplasmic pH (determined by uptake of 5,5-dimethyloxazolidine-2,4-dione). Chlorella cells accumulated [1-14C]IAA from an external solution by pH-sensitive diffusion of IAA across the plasma membrane and anion (IAA−) trapping, but no evidence was found in Chlorella for the occurrence of IAA carriers. These results indicate that carrier systems capable of mediating the transmembrane transport of auxins appeared at a very early stage in the evolution of green plants, possibly in association with the origin of a differentiated, multicellular plant body. Phytotropin receptors evolved independently of the carriers.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- CPP:
-
5-(2-carboxyphenyl)-3-phenylpyrazole
- DMO:
-
5,5-dimethyloxazolidine-2,4-dione
- IAA:
-
indol-3yl-acetic acid
- NPA:
-
N-1-naphthylphthalamic acid
- PBA:
-
2-(1-pyrenoyl)benzoic acid
- TIBA:
-
2,3,5-triiodobenzoic acid
References
Albaum, H.G., Kaiser, S., Nestler, N.A. (1937) The relation of hydrogen-ion concentration to the penetration of 3-indoleacetic acid into Nitella cells. Am. J. Bot. 24, 513–518
Aloni, R. (1987) The induction of vascular tissues by auxin. In: Plant hormones and their role in plant growth and development, pp. 363–374, Davies, P.J., ed. Nijhoff, Dordrecht, The Netherlands
Arisz, W.H. (1969) Intercellular polar transport and the role of plasmodesmata in coleoptiles and Vallisneria leaves. Acta Bot. Neerl. 18, 14–38
Bopp, M., Geier, U. (1988) Protoplasts and transport. In: Methods in bryology. Proc. Bryol. Methods Workshop, Mainz, pp. 89–97, Hattori Bot. Lab., Nichinan
Brennan, T., Jacobs, W.P. (1980) Polarity and the movement of indol-3yl-acetic acid in the coenocyte, Caulerpa prolifera. Ann. Bot. 46, 129–131
Cande, W.Z., Ray, P.M. (1976) Nature of cell-to-cell transfer of auxin in polar transport. Planta 129, 43–52
Davies, P.J., Rubery, P.H. (1978) Components of auxin transport in stem segments of Pisum sativum L. Planta 142, 211–219
Depta, H., Rubery, P.H. (1984) A comparative study of carrier participation in the transport of 2,3,5-triiodobenzoic acid, and 2,4-dichlorophenoxyacetic acid by Cucurbita pepo L. hypocotyl segments. J. Plant Physiol. 115, 371–387
Depta, H., Eisle, K.H., Hertel, R. (1983) Specific inhibition of auxin transport: action on tissue segments and in vitro binding to membranes from maize coleoptiles. Plant Sci. Lett. 31, 181–192
Drake, G., Carr, D.J. (1978) Plasmodesmata, tropisms and auxin transport. J. Exp. Bot. 29, 1309–1318
Edwards, K.L., Goldsmith, M.H.M. (1980) pH-dependent accumulation of indoleacetic acid by corn coleoptile segments. Planta 147, 457–466
Gersani, M., Sachs, T. (1984) Polarity reorientation in beans exressed by vascular differentiation and polar auxin transport. Differentiation 25, 205–208
Goldsmith, M.H.M. (1977) The polar transport of auxin. Annu. Rev. Plant Physiol. 28, 439–478
Goodwin, P.B. (1976) Physiological and electrophysiological evidence for intercellular communication in plant symplasts. In: Intercellular communication in plants: studies on plasmodesmata, pp. 121–129, Gunning, B.E.S., Robards, A.W., eds. Springer, Berlin Heidelberg New York
Jacobs, M., Gilbert, S.F. (1983) Basal localization of the presumptive auxin transport carrier in pea stem cells. Science 220, 1297–1300
Jacobs, M., Short, T.W. (1986) Further characterization of the presumptive auxin transport carrier using monoclonal antibodies. In: Plant growth substances 1985, pp. 218–226, Bopp, M., ed. Springer, Berlin Heidelberg New York
Jacobs, W.P. (1986) Are angiosperm hormones present in, and used by, algae? In: Plant growth substances 1985, pp. 218–226, Bopp, M., ed. Springer, Berlin Heidelberg New York
Jacobs, W.P., Falkenstein, K., Hamilton, R.H. (1985) Nature and amount of auxin in algae: IAA from extracts of Caulerpa paspaloides (Siphonales). Plant Physiol. 78, 844–848
Johnson, C.F., Morris, D.A. (1987) Regulation of auxin transport in pea (Pisum sativum L.) by phenylacetic acid: effects on the components of transmembrane transport of indol-3yl-acetic acid. Planta 172, 400–407
Johnson, C.F., Morris, D.A. (1989) Applicability of the chemiosmotic polar diffusion theory to the transport of indol-3yl-acetic acid in the intact pea (Pisum sativum L.) Planta 178, 242–248
Katekar, G.F., Geissler, A.E. (1977a) Auxin transport inhibitors. II. 2-(1-pyrenoyl)benzoic acid, a potent inhibitor of polar auxin transport. Aust. J. Plant Physiol. 4, 321–325
Katekar, G.F., Geissler, A.E. (1977b) Auxin transport inhibitors. III. Chemical requirements of a class of auxin transport inhibitor. Plant Physiol. 60, 826–829
Katekar, G.F., Geissler, A.E. (1980) Auxin transport inhibitors. IV. Evidence of a common mode of action for a proposed class of auxin transport inhibitors: the phytotropins. Plant Physiol. 66, 1190–1195
Morris, D.A. (1988) Carrier-mediated transmembrane auxin transport: possibilities for regulation and some implications for the control of growth and development. In: Physiology and biochemistry of auxins in plants, pp. 195–203, Kutacek, M., Bandurski, R.S., Krekule, J., eds. Academia, Prague
Morris, D.A., Johnson, C.F. (1985) Characteristics and mechanisms of long-distance auxin transport in intact plants. Acta Univ. Agric. Brno Fac. Agron. 33, 377–384
Morris, D.A., Rubery, P.H., Jarman, J., Sabater, M. (1991) Effects of inhibitors of protein synthesis on transmembrane auxin transport in Cucurbita pepo L. hypocotyl segments. J. Exp. Bot. 42, 773–783
Raven, J.A. (1975) Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its signifiance for polar IAA transport. New Phytol. 74, 163–172
Raven, J.A., Rubery, P.H. (1982) Coordination of development: hormone receptors, hormone action and hormone transport. In: The molecular control of plant development, pp. 28–47, Smith, H., Grierson, D., eds. Blackwells, Oxford
Rose, S., Bopp, M. (1983) Uptake and polar transport of indoleacetic acid in moss rhizoids. Physiol. Plant. 58, 57–61
Rubery, P.H. (1986) The evolution of polar transport models and some possibilities for the regulation of auxin carriers. In: Plant growth substances 1985, pp. 197–202, Bopp, M., ed. Springer, Berlin Heidelberg New York
Rubery, P.H. (1987) Manipulation of hormone transport in physiological and developmental studies. In: Hormone action in plant development — a critical appraisal, pp. 161–174, Hoad, G.V., Lenton, J.P., Jackson, M.B., Atkin, R.K., eds. Butterworths, London
Rubery, P.H. (1990) Phytotropins: receptors and endogenous ligands. Symp. Soc. Exp. Biol. 44, 119–146
Rubery, P.H., Sheldrake, A.R. (1974) Carrier-mediated auxin transport. Planta 118, 101–121
Sabater, M., Sabater, F. (1986) Auxin carriers in membranes of lupin hypocotyls. Planta 167, 76–80
Sachs, T. (1981) Polarity changes and tissue organization in plants. In: Cell biology 1980–1981, pp. 489–496, Schweiger, H.G., ed. Springer, Berlin Heidelberg New York
Sachs, T. (1983) Signal flows as a basis for organized differentiation. In: Biological structures and coupled flows, pp. 457–471, Oplatka, A., Balaban, M., eds. Academic Press, New York
Sachs, T. (1986) Cellular patterns determined by polar transport. In: Plant growth substances 1985, pp. 231–235, Bopp, M. ed., Springer, Berlin Heidelberg New York
Author information
Authors and Affiliations
Additional information
We thank the Nuffield Foundation for the award of an Undergraduate Research Bursary to J.E.D.-F., Dr. G.F. Katekar, C.S.I.R.O., Canberra, Australia for generous gifts of phytotropins, and Mrs. R.P. Bell for technical support.
Rights and permissions
About this article
Cite this article
Dibb-Fuller, J.E., Morris, D.A. Studies on the evolution of auxin carriers and phytotropin receptors: Transmembrane auxin transport in unicellular and multicellular Chlorophyta. Planta 186, 219–226 (1992). https://doi.org/10.1007/BF00196251
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00196251