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Brassinosteroids (BRs) are involved in numerous physiological processes associated with plant development and especially with cell expansion. Here we report that two BRs, 28-homobrassinolide (HBL) and its direct precursor 28-homocastasterone (HCS), promote cell expansion of Arabidopsis thaliana suspension cells. We also show that cell expansions induced by HBL and HCS are correlated with the amplitude of the plasma membrane hyperpolarization they elicited. HBL, which promoted the larger cell expansion, also provoked the larger hyperpolarization. We observed that membrane hyperpolarization and cell expansion were partially inhibited by the proton pump inhibitor erythrosin B, suggesting that proton pumps were not the only ion transport system modulated by the two BRs. We used a voltage clamp approach in order to find the other ion transport systems involved in the PM hyperpolarization elicited by HBL and HCS. Interestingly, while anion currents were inhibited by both HBL and HCS, outward rectifying K+ currents were increased by HBL but inhibited by HCS. The different electrophysiological behavior shown by HBL and HCS indicates that small changes in the BR skeleton might be responsible for changes in bioactivity. © 2005 JSPP.


Documento: Artículo
Título:Brassinosteroids regulate plasma membrane anion channels in addition to proton pumps during expansion of Arabidopsis thaliana cells
Autor:Zhang, Z.; Ramirez, J.; Reboutier, D.; Brault, M.; Trouverie, J.; Pennarun, A.-M.; Amiar, Z.; Biligui, B.; Galagovsky, L.; Rona, J.-P.
Filiación:Laboratoire d'Electrophysiologie des Membranes, EA 3514, Université Paris 7, 2 Place Jussieu, 75251 Paris Cedex 05, France
Departamento de Química Orgánica, Facultad de Ciencias Exactas Y Naturales, Universidad de Buenos Aires, Argentina
Palabras clave:Arabidopsis thaliana; Brassinosteroid; Ion currents; Plasma membrane; Proton pump; Suspension cells; anion; ion channel; proton pump; steroid; Arabidopsis; article; cell membrane; cytology; metabolism; physiology; Anions; Arabidopsis; Cell Membrane; Ion Channels; Proton Pumps; Steroids; Arabidopsis; Arabidopsis thaliana
Página de inicio:1494
Página de fin:1504
Título revista:Plant and Cell Physiology
Título revista abreviado:Plant Cell Physiol.
CAS:Anions; Ion Channels; Proton Pumps; Steroids


  • Axelos, M., Curie, C., Mazzolini, L., Bardet, C., Lescure, B., A protocol for transient gene expression in A. thaliana protoplasts isolated from suspension cultures (1992) Plant Physiol. Biochem., 30, pp. 123-128
  • Barbier-Brygoo, H., Ephritikhine, G., Klämbt, D., Maurel, C., Palme, K., Schell, J., Guern, J., Perception of the auxin signal at the plasma membrane of tobacco mesophyll protoplasts (1991) Plant J., 1, pp. 83-93
  • Bates, G.W., Goldsmith, M.H., Rapid response of the plasmamembrane potential in oat coleoptiles to auxin and other weak acids (1983) Planta, 159, pp. 231-237
  • Bouteau, F., Dellis, O., Rona, J.-P., Transient outward K+ currents across the plasma membrane of laticifer from Hevea brasiliensis (1999) FEBS Lett., 458, pp. 185-187
  • Brault, M., Amiar, Z., Pennarun, A.-M., Monestiez, M., Zhang, Z., Cornel, D., Dellis, O., Rona, J.-P., Plasma membrane depolarization induced by abscisic acid in A. thaliana suspension cells involves reduction of proton pumping in addition to anion channel activation, which are both Ca2+ dependent (2004) Plant Physiol., 135, pp. 231-243
  • Catterou, M., Dubois, F., Schaller, H., Aubanelle, L., Vilcot, B., Sangwan-Norreel, B.S., Sangwan, R.S., Brassinosteroids, microtubules and cell elongaton in A. thaliana. II. Effects of brassinosteroids on microtubules and cell elongation in the bul1 mutant (2001) Planta, 212, pp. 673-683
  • Cerana, R., Bonetti, A., Marrè, M.T., Romani, G., Lado, P., Marrè, E., Effects of a brassinosteroid on growth and electrogenic proton extrusion in Azuki bean epicotyls (1983) Physiol. Plant., 59, pp. 23-27
  • Cho, M.H., Spalding, E.P., An anion channel in Arabidopsis hypocotyls activated by blue light (1996) Proc. Natl Acad. Sci. USA, 93, pp. 134-138
  • Cleland, R.E., Auxin and cell elongation (1995) Plant Hormone, pp. 214-227. , Edited by Davies, P.J. Kluwer Academic Publishers, Dordrecht
  • Clouse, S.D., Brassinosteroid signal transduction: Clarifying the pathway from ligand perception to gene expression (2002) Mol. Cell, 10, pp. 973-982
  • Clouse, S.D., Arabidopsis mutants reveal multiple roles for sterols in plant development (2002) Plant Cell, 14, pp. 1995-2000
  • Clouse, S.D., Sasse, J.M., Brassinosteroids: Essential regulators of plant growth and development (1998) Annu. Rev. Plant Physiol. Plant Mol. Biol., 49, pp. 427-451
  • David, K., Carnero-Diaz, E., Leblanc, N., Monestiez, M., Grosclaude, J., Perrot-Rechenmann, C., Conformational dynamics underlie the activity of the auxin-binding protein, nt-abp1 (2001) J. Biol. Chem., 276, pp. 34517-34523
  • Felle, H., Peters, W., Palme, K., The electrical response of maize to auxins (1991) Biochim. Biophys. Acta, 1064, pp. 199-204
  • Forestier, C., Bouteau, F., Leonhardt, N., Vavasseur, A., Pharmacological properties of slow anion currents in intact guard cells of Arabidopsis. Application of the discontinuous single-electrode voltage-clamp to different species (1998) Pflügers Arch., 436, pp. 920-927
  • Friedrichsen, D., Chory, J., Steroid signaling in plants: From the cell surface to the nucleus (2001) Bioessays, 23, pp. 1028-1036
  • Galagovsky, L.R., Gros, E.G., Ramirez, J.A., Synthesis and bioactivity of natural and C-3 fluorinated biosynthetic precursors of 28-homobrassinolide (2001) Phytochemistry, 58, pp. 973-980
  • Gamborg, O.L., Miller, R.A., Ojima, K., Nutrient requirement of suspension cultures of soybean root cells (1968) Exp. Cell Res., 50, pp. 151-158
  • Ghelis, T., Dellis, O., Jeannette, E., Bardat, F., Cornel, D., Miginiac, E., Rona, J.P., Sotta, B., Abscisic acid specific expression of Rab 18 involves activation of anion channels in Arabidopsis thaliana suspension cells (2000) FEBS Lett., 474, pp. 43-47
  • Goda, H., Shimada, Y., Asami, T., Fujioka, S., Yoshida, S., Microarray analysis of brassinosteroid-regulated genes in Arabidopsis (2002) Plant Physiol., 130, pp. 1319-1334
  • Grove, M.D., Spencer, G.F., Rohwedder, W.K., Mandava, N., Worley, J.F., Warthen Jr., J.D., Steffens, G.L., Cook Jr., J.C., Brassinosteroid, a plant growth-promoting steroid isolated from Brassica napus pollen (1979) Nature, 28, pp. 1216-1217
  • Hallouin, M., Ghelis, T., Brault, M., Bardat, F., Cornel, D., Miginiac, E., Rona, J.P., Jeannette, E., Plasmalemma abscisic acid perception leads to RAB18 expression via phospholipase D activation in Arabidopsis suspension cells (2002) Plant Physiol., 130, pp. 265-272
  • Jeannette, E., Rona, J.P., Bardat, F., Cornel, D., Sotta, B., Miginiac, E., Induction of RAB18 gene expression and activation of K+ outward rectifying channels depend on an extracellular perception of ABA in Arabidopsis thaliana suspension cells (1999) Plant J., 18, pp. 13-22
  • Kasamo, K., Regulation of plasma membrane H+-ATPaSe activity by the membrane environment (2003) J. Plant Res., 16, pp. 517-523
  • Kinoshita, T., Cano-Delgado, A., Seto, H., Hiranuma, S., Fujioka, S., Yoshida, S., Chory, J., Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1 (2005) Nature, 433, pp. 167-171
  • Kurkdjian, A., Bouteau, F., Pennarun, A.M., Convert, M., Cornel, D., Rona, J.P., Bousquet, U., Ion currents involved in early Nod factor responses in Medicago sativa root hairs: A discontinuous single-electrode voltage-clamp study (2000) Plant J., 22, pp. 9-17
  • Li, J.M., Chory, J., A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction (1997) Cell, 90, pp. 929-938
  • Lohse, G., Hedrich, R., Characterization of the plasma membrane H+-ATPase from Vicia faba cells (1992) Planta, 188, pp. 206-214
  • Lohse, G., Hedrich, R., Anions modify the response of guard-cell anion channel to auxin (1995) Planta, 197, pp. 546-552
  • Maeda, E., Rate of lamina inclination in excised rice leaves (1965) Physiol. Plant., 18, pp. 813-827
  • Mandava, N.B., Plant growth-promoting brassinosteroids (1988) Annu. Rev. Plant Physiol. Plant Mol. Biol., 39, pp. 23-53
  • Marten, I., Lohse, G., Hedrich, R., Plant growth hormones control voltage-dependent activity of anion channels in plasma membrane of guard cells (1991) Nature, 353, pp. 759-762
  • Mitchell, J.W., Mandavan, N.B., Worley, J.F., Plimmer, J.R., Smith, M.V., Brassins: A new family of plant hormones from rape pollen (1970) Nature, 255, pp. 1065-1066
  • Morillon, R., Catterou, M., Sangwan, R.S., Sangwan, B.S., Lassalles, J.P., Brassinolide may control aquaporin activities in Arabidopsis thaliana (2001) Planta, 212, pp. 199-204
  • Nemhauser, J.L., Mockler, C.T., Chory, J., Interdependency of brassinosteroid and auxin signaling in Arabidopsis (2004) PLoS Biol., 2, pp. E258
  • Noh, B., Spalding, E.P., Anion channels and the stimulation of anthocyanin accumulation by blue light in Arabidopsis seedlings (1998) Plant Physiol., 116, pp. 503-509
  • Ozga, J.A., Van Huizen, R., Reinecke, D.M., Hormone and seed-specific regulation of pea fruit growth (2002) Plant Physiol., 128, pp. 1379-1389
  • Palmgren, M.G., Plant plasma membrane H+-ATPases: Powerhouses for nutrient uptake (2001) Annu. Rev. Plant Physiol. Mol. Biol., 52, pp. 817-845
  • Ramirez, J.A., Centurión, O.M.T., Gros, E.G., Galagovsky, L.R., Synthesis and bioactivity evaluation of brassinosteroid analogs (2000) Steroids, 65, pp. 329-337
  • Roberts, S.K., Tester, M., Inward and outward K+-selective currents in the plasma membrane of protoplasts from maize root cortex and stele (1995) Plant J., 8, pp. 811-825
  • Romani, G., Marrè, M.T., Bonetti, A., Cerana, R., Lado, P., Marrè, E., Effects of a brassinosteroid on growth and electrogenic proton extrusion in maize root segments (1983) Physiol. Plant., 59, pp. 528-532
  • Sasse, J.M., Brassinolide-induced elongation and auxin (1990) Physiol. Plant., 80, pp. 401-408
  • Schaller, H., The role of sterols in plant growth and development (2003) Prog. Lipid Res., 42, pp. 163-175
  • Schroeder, J.I., Anion channels as central mechanisms for signal transduction in guard cells and putative functions in roots for plant-soil interactions (1995) Plant Mol. Biol., 28, pp. 353-361
  • Schroeder, J.I., Allen, G.I., Hugouvieux, V., Kwak, J.M., Warner, D., Guard cell signal transduction (2001) Annu. Rev. Plant Physiol. Plant Mol. Biol., 52, pp. 627-658
  • Schroeder, J.I., Keller, B.U., Two types of anion channel currents on guard cells with distinct voltage regulation (1992) Proc. Natl Acad. Sci. USA, 89, pp. 5025-5029
  • Schumacher, K., Vafeados, D., McCarthy, M., Sze, H., Wilkins, T., Chory, J., The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development (1999) Genes Dev., 13, pp. 3259-3270
  • Schwartz, A., Ilan, N., Schwarz, M., Scheaffer, J., Assmann, S.M., Schroeder, J.I., Anion-channel blockers inhibit S-type anion channels and abscisic acid responses in guard cells (1995) Plant Physiol., 109, pp. 651-658
  • Serrano, R., Structure and function of plasma membrane ATPase (1989) Annu. Rev. Plant Physiol. Plant Mol. Biol., 40, pp. 61-94
  • Shimaoka, T., Ohnishi, M., Sazuka, T., Mitsuhashi, N., Hara-Nishimura, I., Shimazaki, K., Maeshima, M., Mimura, T., Isolation of intact vacuoles and proteomic analysis of tonoplast from suspension-cultured cells of Arabidopsis thaliana (2004) Plant Cell Physiol., 45, pp. 672-683
  • Sondergaard, T.E., Schulz, A., Palmgren, M.G., Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase (2004) Plant Physiol., 136, pp. 2475-2482
  • Sze, H., Li, X., Palmgren, M.G., Energization of plant cell membranes by H+-pumping ATPases: Regulation and biosynthesis (1999) Plant Cell, 11, pp. 677-689
  • Teme Centurión, O.M., Galagovsky, L.R., Alternative synthesis of 24(S)-homoethylcastasterone from stigmasterol (1998) Anal. Asoc. Quím. Argentina, 86, pp. 104-109
  • Thomine, S., Lelièvre, F., Boufflet, M., Guern, J., Barbier-Brygoo, H., Anion-channel blockers interfere with auxin responses in dark-grown Arabidopsis hypocotyls (1997) Plant Physiol., 115, pp. 533-542
  • Thummel, C.S., Chory, J., Steroid signaling in plants and insects - Common themes, different pathways (2002) Genes Dev., 15, pp. 3113-3129
  • Tode, K., Lüthen, H., Fusicoccin- and IAA-induced elongation growth share the same pattern of K+ dependence (2001) J. Exp. Bot., 52, pp. 251-255
  • Vardhini, B.V., Rao, S.S., Acceleration of ripening of tomato pericarp discs by brassinosteroids (2002) Phytochemistry, 16, pp. 843-847
  • Wach, A., Gräber, P., The plasma membrane H+ -ATPase from yeast: Effects of pH, vanadate and erythrosin B on ATP hydrolysis and ATP binding (1991) Eur. J. Biochem., 201, pp. 91-97
  • Wang, X.J., Iino, M., Blue-light-induced shrinking of protoplasts from maize coleoptiles and its relationship to coleoptile growth (1997) Plant Physiol., 114, pp. 1009-1020
  • Wang, X.J., Iino, M., Interaction of cryptochrome 1, phytochrome, and ion fluxes in blue-light-induced shrinking of Arabidopsis hypocotyls protoplasts (1998) Plant Physiol., 117, pp. 1265-1279
  • Wang, Z.Y., He, J.X., Brassinosteroid signal-transduction - Choices of signals and receptors (2004) Trends Plant Sci., 9, pp. 91-96
  • Xu, W., Purugganan, M.M., Polisenksy, D.H., Antosiewicz, D.M., Fry, S.C., Braam, J., Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase (1995) Plant Cell, 7, pp. 1555-1567
  • Zimmermann, S., Thomine, S., Guern, J., Barbier-Brygoo, H., An anion current at the plasma membrane of tobacco protoplasts shows ATP-dependent voltage regulation and is modulated by auxin (1994) Plant J., 6, pp. 707-716
  • Zingarelli, L., Marrè, M.T., Massardi, F., Lado, P., Effects of hyperosmotic stress on K+ fluxes, H+ extrusion, transmembrane electric potential difference and comparison with the effects of fusicoccin (1999) Physiol. Plant., 106, pp. 287-295
  • Zonia, L., Cordeiro, S., Tupy, J., Feijo, J.A., Oscillatory chloride efflux at the pollen tube apex has a role in growth and cell volume regulation and is targeted by inositol 3, 4, 5, 6-tetrakisphosphate (2002) Plant Cell, 14, pp. 2233-2249
  • Zurek, D.M., Rayle, D.L., McMorris, T.C., Clouse, S.D., Investigation of gene expression, growth kinetics, and wall extensibility during brassinosteroid-regulated stem elongation (1994) Plant Physiol., 104, pp. 505-513


---------- APA ----------
Zhang, Z., Ramirez, J., Reboutier, D., Brault, M., Trouverie, J., Pennarun, A.-M., Amiar, Z.,..., Rona, J.-P. (2005) . Brassinosteroids regulate plasma membrane anion channels in addition to proton pumps during expansion of Arabidopsis thaliana cells. Plant and Cell Physiology, 46(9), 1494-1504.
---------- CHICAGO ----------
Zhang, Z., Ramirez, J., Reboutier, D., Brault, M., Trouverie, J., Pennarun, A.-M., et al. "Brassinosteroids regulate plasma membrane anion channels in addition to proton pumps during expansion of Arabidopsis thaliana cells" . Plant and Cell Physiology 46, no. 9 (2005) : 1494-1504.
---------- MLA ----------
Zhang, Z., Ramirez, J., Reboutier, D., Brault, M., Trouverie, J., Pennarun, A.-M., et al. "Brassinosteroids regulate plasma membrane anion channels in addition to proton pumps during expansion of Arabidopsis thaliana cells" . Plant and Cell Physiology, vol. 46, no. 9, 2005, pp. 1494-1504.
---------- VANCOUVER ----------
Zhang, Z., Ramirez, J., Reboutier, D., Brault, M., Trouverie, J., Pennarun, A.-M., et al. Brassinosteroids regulate plasma membrane anion channels in addition to proton pumps during expansion of Arabidopsis thaliana cells. Plant Cell Physiol. 2005;46(9):1494-1504.