Abstract
Microsomal vesicles were prepared from zucchini (Cucurbita pepo L.) hypocotyls containing radioactive phosphatidylethanolamine or phosphatidylcholine, and these lipids were used as substrates by phospholipase A which is activated by auxins. Phospholipase D and phospholipase C hydrolysed the same substrates but were not influenced by auxin. Phospholipase A was activated by the auxins indolyl-3-acetic acid, 2,4-dichlorophenoxyacetic acid and, to a lesser extent, by α-naphthaleneacetic acid whereas the weak auxins 2,3-dichlorophenoxyacetic acid and β-naphthaleneacetic acid were almost inactive. This hormone specificity was also found in growth tests with etiolated zucchini hypocotyls. Phospholipase A activation by auxin was blocked by a polyclonal antibody against the maize auxin-binding protein. We propose that phospholipase A activation is a primary reaction in the signal transduction leading from hormone-binding to the growth response.
Similar content being viewed by others
Abbreviations
- IAA:
-
indolyl-3-acetic acid
- 2,3-D, 2,4-D:
-
2,3- and 2,4-dichlorophenoxyacetic acid
- α-NAA; β-NAA:
-
α- and β-naphthaleneacetic acid
References
Barbier-Brygoo, H., Ephritikine, G., Klämbt, D., Ghislain, M., Guern, J. (1989) Functional evidence for an auxin receptor at the plasmalemma of tobacco mesophyll protoplasts. Proc. Natl. Acad. Sci. USA 86, 891–895
Batt, S., Wilkins, M.B., Venis, M.A. (1976) Auxin binding to corn coleoptile membranes: kinetics and specificity. Planta 130, 7–13
Berridge, M.J. (1987) Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu. Rev. Biochem. 56, 159–163
Bligh, E.G., Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917
Brooks, R.C., McCarthy, K.D., Lapetina, E.G., Morell, P. (1989) Receptor-stimulated phospholipase A2 activation is coupled to influx of external calcium and not to mobilization of intracellular calcium in C62B glioma cells. J. Biol. Chem. 264, 20147–20153
Burch, R.M., Luini, A., Axelrod J. (1986) Phospholipase A2 and phospholipase C are activated by distinct GTP-binding proteins in response to α-adrenergic stimulation of FRTL5 thyroid cells. Proc. Natl. Acad. Sci. USA 83, 7201–7205
Burch, R.M., Connor, J.R., Axelrod, J. (1988) Interleukin amplifies receptor-mediated activation of phospholipase A2 in 3T3 cells. Proc. Natl. Acad. Sci. USA 85, 6306–6309
Cleland, R.E (1973) Auxin-induced hydrogen ion excretion from Avena coleoptiles. Proc. Natl. Acad. Sci. USA 70, 3092–3093
Ettlinger, C, Lehle, L. (1988) Auxin induces rapid changes in phosphatidylinositol metabolites. Nature 331, 176–178
Exton, J.H. (1990) Signaling through phosphatidylcholine breakdown. J. Biol. Chem. 265, 1–4
Evans, M.J. (1974) Rapid responses to plant hormones. Annu. Rev. Plant Physiol. 25, 195–223
Gabathuler, R., Cleland, R.E. (1985) Auxin regulation of a proton translocating ATPase in pea root plasma membrane vesicles. Plant Physiol. 79, 1080–1085
Hager, A., Menzel, H., Kraus, A. (1971) Versuche und Hypothese zur Primärwirkung des Auxins beim Streckungswachstum. Planta 100, 47–75
Hager, A., Brich, M., Debus, G., Edel, H.G., Priester G. (1989) Membrane metabolism and growth. Phospholipases, protein kinases and exocytotic processes in coleoptiles in Zea mays. In: Plant Water Relations and Growth under Stress, pp. 275–282. Yamada Science Foundation, Osaka Tokyo
Heim, S., Wagner, K.G. (1989) Inositol phosphates in the growth cycle of suspension cultured plant cells. Plant Sci. 63, 159–165
Hesse, T., Feldwisch, J., Balshüsemann, D., Bauw, G., Puype, M., Vandekerkhove, J., Löbler, M., Klämbt, D., Schell, J., Palme, J. (1989) Molecular cloning and structural analysis of a gene from Zea mays (L.) coding for a putative receptor for the plant hormone auxin. EMBO J. 8, 2453–2461
Inohara, N., Shimomura, S., Fukui, T., Futai, M. (1989) Auxin-binding protein located in the endoplasmic reticulum of maize shoots: molecular cloning and complete primary structure. Proc. Natl. Acad. Sci. USA 86, 3564–3568
Jelsema, C.A. (1987) Light-induced changes of phospholipase A2 in rod outer segments and its modulation by GTP-binding proteins. J. Biol. Chem. 262, 163–168
Kasamo, K., Yamaki, T. (1974) Effect of auxin on Mg2+-activated and inhibited ATPase from mung bean hypocotyls. Plant Cell Physiol. 52, 60–87
Kutschera, U., Bergfeld, R., Schopfer, P. (1987) Cooperation of epidermis and inner tissues in auxin-mediated growth of maize coleoptiles. Planta 170, 168–180
Löbler, M., Klämbt, D. (1985) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). J. Biol. Chem. 260, 9848–9853
Martiny-Baron, G., Scherer, G.F.E. (1989) Phospholipid-stimulated protein kinase in plants. J. Biol. Chem. 264, 18052–18059
Morré, D.J. (1989) Stimulus-response coupling in auxin regulation of plant cell elongation. In: Second messengers in plant growth and development, pp. 81–114, Boss, W.F., Morré, D.J., eds. Alan Liss, New York
Morré, D.J., Pfaffmann, H., Drobes, B., Wilkinson, F.E., Hartmann, E. E. (1989) Diacylglycerol levels unchanged during auxin-stimulated growth of excised hypocotyl segments of soybean. Plant Physiol. 90, 275–279
Murayama, T., Kajiyama, Y., Nomura, Y. (1990) Histamine-stimulated and GTP-binding proteins-mediated phospholipase A2 activation in rabbit platelets. J. Biol. Chem. 265, 4290–4295
Nishizuka, Y. (1986) Studies and perspectives of protein kinase C. Science 233, 305–317
Ogita, K., Miyamoto, S., Koide, H., Iwai, T., Oka, M., Ando, K., Kishimoto, A., Ikeda, K., Fukami, Y, Nishizuka, Y. (1990) Protein kinase C in Saccharomyces cerevisiae: Comparison with the mammalian enzyme. Proc. Natl. Acad. Sci. USA 87, 5011–5015
Palmgren, M.G., Sommarin, M. (1989) Lysophosphatidylcholine stimulates ATP-dependent proton accumulation in isolated oat root plasma membrane vesicles. Plant Physiol. 90, 1009–1014
Pelech, S.L., Vance, D.E. (1989) Signal transduction via phosphatidylcholine cycles. Trends Biochem. Sci. 14, 28–30
Ray, P.M., Dohrmann, U., Hertel, R. (1977) Specificity of auxin-binding sites on maize coleoptile membranes as possible receptor sites for auxin. Plant Physiol. 60, 585–591
Rozengurt, E. (1986) Early signals in the mitogenic response. Science 234, 161–166
Santoni, V., Vansuyt, G., Rossignol, M. (1990) Auxin sensitivity of the plasma membrane H+-ATPase and induction to flowering. Physiol. Plant. 79, A33
Schaller, G.E., Sussman M.G. (1988) Phosphorylation of the plasma membrane H+-ATPase of oat roots by calcium-stimulated protein kinase. Planta 173, 509–518
Scherer, G.F.E. (1981) Auxin-stimulated ATPase in membrane fractions from pumpkin hypocotyls (Cucurbita maxima L.). Planta 151, 434–438
Scherer, G.F.E. (1984) Stimulation of ATPase activity is dependent on ATP concentration. Planta 161, 394–397
Scherer, G.F.E. (1985) 1-O-alkyl-2-acetyl-sn-glycero-3-phosphocholine (platelet-activating factor) stimulates plant H+ transport and growth. Biochem. Biophys. Res. Commun. 133, 1160–1167
Scherer, G.F.E. (1990) Phospholipid-activated protein kinase in plants: coupled to phospholipase A2? In: Signal perception and transduction in higher plants, NATO-ASI Ser. H, vol. 47, pp. 69–82, Ranjeva, R., Boudet, A.M., eds. Springer, Berlin Heidelberg New York
Scherer, G.F.E., André, B. (1989) A rapid response to a plant hormone: auxin stimulates phospholipase A2 in vivo and in vitro. Biochem. Biophys. Res. Commun. 163, 111–117
Scherer, G.F.E., Morré, D.J. (1978) In vitro stimulation by 2,4-dichlorophenoxyactic acid of an ATPase and inhibition of phosphatidate phosphatase of plant membranes. Biochem. Biophys. Res. Commun. 84, 238–247
Scherer, G.F.E., Nickel (1988) The animal ether phospholipid platelet-activating factor stimulates acidification of the incubation medium by cultured soybean cells. Plant Cell Rep. 7, 575–578
Scherer, G.F.E., Martiny-Baron, G., Stoffel, B. (1988) A new set of regulatory molecules in plants: a plant phospholipid similar to platelet-activating factor stimulates protein kinase and proton-translocating ATPase in membrane vesicles. Planta 175, 241–253
Scherer, G.F.E., André, B., Martiny-Baron, G. (1990) Hormone-activated phospholipase A2 and lysophospholipid-activated protein kinase: a new signal transduction chain and a new second messenger system in plants? Current Top. Plant Biochem. Physiol. 9, 190–218
Serrano, R., Montesinos, C., Sanchez, J. (1988) Lipid requirements of the plasma membrane ATPase from oat roots and yeast. Plant Sci. 56, 117–122
Shou-Peng, L., Jin-Shan, L. (1983) Regulation of potassium uptake in etiolated sunflower hypocotyl segments by indole-3-acetic acid. Acta Phytophysiol. Sin. 9, 391–402
Sibley, D.R., Benovic, J.L., Caron, M.G., Lefkowitz, R.J. (1987) Regulation of transmembrane signaling by receptor phosphorylation. Cell 48, 913–922
Silk, S.T., Clejan, S., Witkom, K. (1989) Evidence of GTP-binding protein regulation of phospholipase A2 activity in isolated human platelet membranes. J. Biol. Chem. 264, 21466–21469
Teitelbaum, I. (1990) The epidermal growth factor receptor is coupled to a phospholipase A2-specific pertussis toxin-inhibitable guanine nucleotide-binding regulatory protein in cultured inner medullary collecting tubule cells. J. Biol. Chem. 265, 4218–4222
Theologis, A. (1986) Rapid gene regulation by auxin. Annu. Rev. Plant Physiol. 37, 407–438
Thimann, K.V. (1972) Hormone action in the whole life of plants. University of Massachusetts Press, Cambridge
Tillmann, U., Viola, G., Kayser, B., Siemeister, G., Hesse, T., Palme, K., Löbler, M., Klämbt D. (1989) cDNA clones of the auxin-binding protein from corn coleoptiles (Zea mays L.): isolation and characterization by immunological methods. EMBO J. 8, 2463–2467
Zbell, B., Walter-Back, C. (1988) Signal transduction of auxin on isolated plant cell membranes: indications for a rapid polyphosphoinositide response stimulated by indoleacetic acid. J. Plant Physiol. 133, 353–360
Author information
Authors and Affiliations
Additional information
This work was supported by the Deutsche Forchungsgemeinschaft. We thank D. Klämbt (Botanical Institute, University of Bonn, FRG) for a generous gift of polyclonal antibody (IgG fraction) against auxin-binding protein and U. Kutschera (Botanical Institute, University of Bonn, FRG) for advice with the growth tests.
Rights and permissions
About this article
Cite this article
André, B., Scherer, G.F.E. Stimulation by auxin of phospholipase A in membrane vesicles from an auxin-sensitive tissue is mediated by an auxin receptor. Planta 185, 209–214 (1991). https://doi.org/10.1007/BF00194062
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00194062