Ca2plus/Hplus exchange in the plasma membrane of Arabidopsis thaliana leaves

• Autorzy: Zhai J. , Xu H. , Cong X. , Deng Y. , Xia Z. , Huang X. , Hao G. , Jiang X.
• Języki publikacji: EN

Abstrakty

EN

A large number of plant Ca2+/H+ exchangers have been identified in endomembranes, but far fewer have been studied for Ca2+/H+ exchange in plasma membrane so far. To investigate the Ca2+/H+ exchange in plasma membrane here, inside-out plasma membrane vesicles were isolated from Arabidopsis thaliana leaves using aqueous two-phase partitioning method. Ca2+/H+ exchange in plasma membrane vesicles was measured by Ca2+-dependent dissipation of a pre-established pH gradient. The results showed that transport mediated by the Ca2+/H+ exchange was optimal at pH 7.0, and displayed transport specificity for Ca2+ with saturation kinetics at Km = 47 lM. Sulfate and vanadate inhibited pH gradient across vesicles and decreased the Ca2+-dependent transport of H+ out of vesicles significantly. When the electrical potential across plasma membrane was dissipated with valinomycin and potassium, the rate of Ca2+/H+ exchange increased comparing to control without valinomycin effect, suggesting that the Ca2+/H+ exchange generated a membrane potential (interior negative), i.e. that the stoichiometric ratio for the exchange is greater than 2H+:Ca2+. Eosin Y, a Ca2+-ATPase inhibitor, drastically inhibited Ca2+/H+ exchange in plasma membrane as it does for the purified Ca2+-ATPase in proteoliposomes, indicating that measured Ca2+/H+ exchange activity is mainly due to a plasma membrane Ca2+ pump. These suggest that calcium (Ca2+) is transported out of Arabidopsis cells mainly through a Ca2+-ATPase-mediated Ca2+/H+ exchange system that is driven by the proton-motive force from the plasma membrane H+-ATPase.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2013
• Tom: 35
• Numer: 01
• Opis fizyczny: p.161-173,fig.,ref.

Twórcy

autor

Zhai J.

• Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources/Institute of Bioscience and Technology, College of Agriculture, Hainan University, Haikou 570228, China

autor

Xu H.

• College of Agronomy, Henan Agricultural University, Zhengzhou 450002, China

autor

Cong X.

• Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources/Institute of Bioscience and Technology, College of Agriculture, Hainan University, Haikou 570228, China

autor

Deng Y.

• Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources/Institute of Bioscience and Technology, College of Agriculture, Hainan University, Haikou 570228, China

autor

Xia Z.

• Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources/Institute of Bioscience and Technology, College of Agriculture, Hainan University, Haikou 570228, China

autor

Huang X.

• Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources/Institute of Bioscience and Technology, College of Agriculture, Hainan University, Haikou 570228, China

autor

Hao G.

• Institute of Medicinal Biotechnology, Taishan Medical University, Taian 271000, China

autor

Jiang X.

• Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources/Institute of Bioscience and Technology, College of Agriculture, Hainan University, Haikou 570228, China

Bibliografia

• Anil VS, Rajkumar P, Kumar P, Mathew MK (2008) A plant Ca2+ pump, ACA2, relieves salt hypersensitivity in yeast. Modulation of cytosolic calcium signature and activation of adaptive Na+ homeostasis. J Biol Chem 283:3497–3506
• Beffagna N, Romani G, Sforza MC (2000) H+fluxes at plasmalemma level: in vivo evidence for a significant contribution of the Ca2+- ATPase and for the involvement of its activity in the abscisic acid-induced changes in Egeria densa leaves. Plant Biol 2:168–175
• Blackford S, Rea PA, Sanders D (1990) Voltage sensitivity of H+/ Ca2+antiport in higher plant tonoplast suggests a role in vacuolar calcium accumulation. J Biol Chem 265:9617–9620
• Blumwald E, Poole RJ (1986) Kinetics of Ca2+/H+antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris L. Plant Physiol 80:727–731
• Bonza MC, Morandini P, Luoni L, Geisler M, Palmgren MG, De Michelis MI (2000) At-ACA8 encodes a plasma membranelocalized calcium-ATPase of Arabidopsis with a calmodulinbinding domain at the N terminus. Plant Physiol 123:1495–1506
• Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
• Briskin DP, Leonard RT, Hodges TK (1987) Isolation of the plasma membrane: membrane markers and general principles. Methods Enzymol 148:542–559
• Catala R, Santos E, Alonso JM, Ecker JR, Martinez-Zapater JM, Salinas J (2003) Mutations in the Ca2+/H+transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940–2951
• Cheng NH, Hirschi KD (2003) Cloning and characterization of CXIP1, a novel PICOT domain-containing Arabidopsis protein that associates with CAX1. J Biol Chem 278:6503–6509
• Cheng NH, Pittman JK, Shigaki T, Hirschi KD (2002) Characterization of CAX4, an Arabidopsis H+/cation antiporter. Plant Physiol 128:1245–1254
• Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404
• Edmond C, Shigaki T, Ewert S, Nelson MD, Connorton JM, Chalova V, Noordally Z, Pittman JK (2009) Comparative analysis of CAX2-like cation transporters indicates functional and regulatory diversity. Biochem J 418:145–154
• Evans DE, Briars SA, Williams LE (1991) Active calcium transport by plant cell membranes. J Exp Bot 42:285–303
• Gallet O, Lemoine R, Larsson C, Delrot S (1989) The sucrose carrier of the plant plasma membrane. I. Differential affinity labeling. Biochim Biophys Acta Biomembranes 978(1):56–64
• Giannini JL, Holt JS, Briskin DP (1988) Isolation of sealed plasma membrane vesicles from Phytophthora megasperma f. sp. glycinea: II. Partial characterization of Ca2+transport and glyceollin effects. Arch Biochem Biophys 266:644–649
• Gilroy S, Jones RL (1992) Gibberellic acid and abscisic acid coordinately regulate cytoplasmic calcium and secretory activity in barley aleurone protoplasts. Proc Natl Acad Sci USA 89:3591–3595
• Guo KM, Babourina O, Christopher DA, Borsic T, Rengel Z (2010) The cyclic nucleotide-gated channel AtCNGC10 transports Ca2+ and Mg2+in Arabidopsis. Physiol Plant 139:303–312
• Hepler PK, Winship LJ (2010) Calcium at the cell wall-cytoplast interface. J Integr Plant Biol 52(2):147–160
• Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122
• Hirschi KD (2001) Vacuolar H+/Ca2+transport: who’s directing the traffic+Trends Plant Sci 6:100–104
• Hirschi KD, Zhen RG, Cunningham KW, Rea PA, Fink GR (1996) CAX1, an H+/Ca2+antiporter from Arabidopsis. Proc Natl Acad Sci USA 93:8782–8786
• Hirschi KD, Korenkov VD, Wilganowski NL, George J, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–134
• Ivey DM, Guffanti AA, Zemsky J, Pinner E, Karpel R, Padan E, Schuldiner S, Krulwich TA (1993) Cloning and characterization of a putative Ca2+/H+ antiporter gene from Escherichia coli upon functional complementation of Na+/H+ antiporter-deficient strains by the overexpress gene. J Biol Chem 268:11296–11303
• Johansson F, Olbe M, Sommarin M, Larsson C (1995) Brij58, a polyoxyethylene acyl ether, creates membrane vesicles of uniform sidedness. A new tool to obtain inside-out (cytoplasmic side-out) plasma membrane vesicles. Plant J 7:165–173
• Kasai M, Muto S (1990) Ca2+ pump and Ca2+/H+ antiporter in plasma membrane vesicles isolated by aqueous two-phase partitioning from corn leaves. J Membrane Biol 114:133–142
• Körner LE, Kjellbom P, Larsson C, Møller IM (1985) Surface properties of right side-out plasma membrane vesicles isolated from barley roots and leaves. Plant Physiol 79(1):72–79
• Llinas R, Subimori M, Silver RB (1992) Microdomains of high calcium concentration in a presynaptic terminal. Science 256:677–679
• Luo GZ, Wang HW, Huang J, Tian AG, Wang YJ, Zhang JS, Chen SY (2005) A putative plasma membrane cation/proton antiporter from soybean confers salt tolerance in Arabidopsis. Plant Mol Biol 59:809–820
• Luoni L, Bonza MC, De Michelis MI (2000) H+/Ca2+ exchange driven by the plasma membrane Ca2+-ATPase of Arabidopsis thaliana reconstituted in proteoliposomes after calmodulinaffinity purification. FEBS Lett 482:225–230
• Luoni L, Meneghelli S, Bonza MC, De Michelis MI (2004) Autoinhibition of Arabidopsis thaliana plasma membrane Ca2+- ATPase involves an interaction of the N-terminus with the small cytoplasmic loop. FEBS Lett 574:20–24
• Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJM, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667
• Maurousset L, Lemoine R, Gallet O, Delrot S, Bonnemain JL (1992) Sulfur dioxide inhibits the sucrose carrier of the plant plasma membrane. Biochim Biophys Acta Biomembranes 1105(2):230–236
• McAinsh MR, Hetherington AM (1998) Encoding specificity in Ca2+ signaling systems. Trends Plant Sci 3:32–36
• McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294
• Menendez A, Larsson C, Ugalde U (1995) Purification of functionally sealed cytoplasmic side-out plasma membrane vesicles from Saccharomyces cerevisiae. Anal Biochem 230:308–314
• Migocka M, Klobus G (2007) The properties of the Mn, Ni and Pb transport operating at plasma membranes of cucumber roots. Physiol Plant 129:578–587
• Moreno I, Norambuena L, Maturana D, Toro M, Vergara C, Orellana A, Zurita-Silva A, Ordenes VR (2008) AtHMA1 is a thapsigargin-sensitive Ca2+/heavy metal pump. J Biol Chem 283:9633–9641
• Pineros M, Tester M (1997) Characterization of the high-affinity verapamil binding site in a plant plasma membrane Ca2+- selective channel. J Membrane Biol 157:139–145
• Pittman JK, Hirschi KD (2001) Regulation of CAX1, an Arabidopsis Ca2+/H+ antiporter. Identification of an N-terminal autoinhibitory domain. Plant Physiol 127:1020–1029
• Pittman JK, Sreevidya CS, Shigaki T, Ueoka-Nakanishi H, Hirschi KD (2002) Distinct N-terminal regulatory domains of Ca2+/H+ antiporters. Plant Physiol 130:1054–1062
• Pottosin II, Schönknecht G (2007) Vacuolar calcium channels. J Exp Bot 58:1559–1569
• Qi Z, Stephens NR, Spalding EP (2006) Calcium entry mediated by GLR3.3, an Arabidopsis glutamate receptor with a broad agonist profile. Plant Physiol 142:963–971
• Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad of Sci USA 99:8436–8441
• Qiu QS, Barkla BJ, Vera-Estrella R, Zhu JK, Schumaker KS (2003) Na+/H+ exchange activity in the plasma membrane of Arabidopsis. Plant Physiol 132:1041–1052
• Qudeimata E, Faltusza AMC, Wheeler G, Lang D, Brownlee C, Reskia R, Frank W (2008) A PIIB-type Ca2+-ATPase is essential for stress adaptation in Physcomitrella patens. Proc Natl Acad Sci USA 105:19555–19560
• Ranf S, Wunnenberg P, Lee J, Becker D, Dunkel M, Hedrich R, Scheel D, Dietrich P (2008) Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses. Plant J 53:287–299
• Rasi-Caldogno F, Pugliarello M, De Michelis MI (1987) The Ca2+- transport ATPase of plant plasma membrane catalyzes a nH+/ Ca2+ exchange. Plant Physiol 83:994–1000
• Salvador JM, Inesi G, Rigaud JL, Mata AM (1998) Ca2+ Transport by reconstituted synaptosomal ATPase is associated with H+ countertransport and net charge displacement. J Biol Chem 273:18230–18234
• Schiott M, Romanowsky SM, Bækgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101:9502–9507
• Schumaker KS, Sze H (1990) Solubilization and reconstitution of the oat root vacuolar H+/Ca2+ exchanger. Plant Physiol 92:340–345
• Shigaki T, Hirschi KD (2006) Diverse functions and molecular properties emerging for CAX cation/H+exchanger in plants. Plant Biol 8:419–429
• Shigaki T, Cheng NH, Pittman JK, Hirschi KD (2001) Structural determination of Ca2+transport in the Arabidopsis H+/Ca2+ antiporter CAX1. J Biol Chem 276:43152–43159
• Shigaki T, Rees I, Nakhelh L, Hirschi KD (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815–825
• Spalding EP, Harper JF (2011) The ins and outs of cellular Ca(2+) transport. Curr Opin Plant Biol 14:715–720
• Ueoka-Nakanishi H, Nakanishi Y, Tanaka Y, Maeshima M (1999) Properties and molecular cloning of Ca2+/H+antiporter in the vacuolar membrane of mung bean. Eur J Biochem 262:417–425
• Veresov VG, Kabak AG, Volotovsky ID (2003) Modeling the calcium signaling in stomatal guard cells under the action of abscisic acid. Russ J Plant Physiol 50:573–579
• Vicente JAF, Vale MGP (1995) Activities of Ca2+pump and low affinity Ca2+/H+antiport in plasma membrane vesicles of corn roots. J Exp Bot 46:1551–1559
• Waditee R, Hossain GS, Tanaka Y, Nakamura T, Shikata M, Takano J, Takabe T (2004) Isolation and functional characterization of Ca2+/H+antiporters from cyanobacteria. J Biol Chem 279:4330–4338
• Weinl S, Kudla J (2009) The CBL–CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528
• White PJ (1998) Calcium channels in the plasma membrane of root cells. Ann Bot 81:173–183
• Zhu X, Caplan J, Mamillapalli P, Czymmek K, Dinesh-Kumar SP (2010) Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death. EMBO J 29:1007–1018

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