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Ca2+ Pumps and Ca2+ Antiporters in Plant Development

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Transporters and Pumps in Plant Signaling

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 7))

Abstract

Calcium (Ca2+) efflux transporters remove Ca2+ from the cytosol of the cell either by transporting it out of the cell across the plasma membrane or into internal organelles. These transporters, which include Ca2+-ATPases and Ca2+/H+ antiporters, have a critical role in preventing Ca2+ toxicity, maintaining cytosolic Ca2+ at a low resting level, and transferring Ca2+ to specific cellular locations where it is required. Many genes encoding plant Ca2+-ATPases and Ca2+/H+ antiporters have now been identified and characterised to elucidate their biochemical and genetic features. Furthermore, the use of gene knockouts has begun to provide evidence for an involvement of these Ca2+ transporters in Ca2+-signaling networks and in various aspects of plant development.

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References

  • Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342

    Article  PubMed  CAS  Google Scholar 

  • Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffman T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Askerlund P (1997) Calmodulin-stimulated Ca2+-ATPases in the vacuolar and plasma membranes in cauliflower. Plant Physiol 114:999–1007

    Article  PubMed  CAS  Google Scholar 

  • Askerlund P, Sommarin M (1996) Calcium efflux transporters in higher plants. In: Smallwood M, Knox JP, Bowles DJ (eds) Membranes: specialized functions in plants. BIOS Scientific Publishers, Oxford, pp 281–299

    Google Scholar 

  • Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101

    Article  PubMed  CAS  Google Scholar 

  • Bækgaard L, Luoni L, De Michelis MI, Palmgren MG (2006) The plant plasma membrane Ca2+ pump ACA8 contains overlapping as well as physically separated autoinhibitory and calmodulin-binding domains. J Biol Chem 281:1058–1065

    Article  PubMed  CAS  Google Scholar 

  • Barkla BJ, Hirschi KD, Pittman JK (2008) Exchangers man the pumps: functional interplay between proton pumps and proton-coupled Ca2+ exchangers. Plant Signal Behav 3:354–356

    Article  PubMed  Google Scholar 

  • Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618–628

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Benjamins R, Ampudia CSG, Hooykaas PJJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bonza C, Carnelli A, De Michelis MI, Rasi-Caldogno F (1998) Purification of the plasma membrane Ca2+-ATPase from radish seedlings by calmodulin-agarose affinity chromatography. Plant Physiol 116:845–851

    Article  PubMed  CAS  Google Scholar 

  • Bonza MC, Morandini P, Luoni L, Geisler M, Palmgren MG, De Michelis MI (2000) At-ACA8 encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiol 123:1495–1505

    Article  PubMed  CAS  Google Scholar 

  • Bonza MC, Luoni L, De Michelis MI (2001) Stimulation of plant plasma membrane Ca2+-ATPase activity by acidic phospholipids. Physiol Plant 112:315–320

    Article  PubMed  CAS  Google Scholar 

  • Bonza MC, Luoni L, De Michelis MI (2004) Functional expression in yeast of an N-deleted form of At-ACA8, a plasma membrane Ca2+-ATPase of Arabidopsis thaliana, and characterization of a hyperactive mutant. Planta 218:814–823

    Article  PubMed  CAS  Google Scholar 

  • Boursiac Y, Harper JF (2007) The origin and function of calmodulin regulated Ca2+ pumps in plants. J Bioenerg Biomembr 39:409–414

    Article  PubMed  CAS  Google Scholar 

  • Bredeston LM, Adamo HP (2004) Loss of autoinhibition of the plasma membrane Ca2+ pump by substitution of aspartic 170 by asparagine – activation of plasma membrane calcium ATPase 4 without disruption of the interaction between the catalytic core and the C-terminal regulatory domain. J Biol Chem 279:41619–41625

    Article  PubMed  CAS  Google Scholar 

  • Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89:1341–1378

    Article  PubMed  CAS  Google Scholar 

  • Bush DR, Sze H (1986) Calcium-transport in tonoplast and endoplasmic-reticulum vesicles isolated from cultured carrot cells. Plant Physiol 80:549–555

    Article  PubMed  CAS  Google Scholar 

  • Cai XJ, Lytton J (2004) The cation/Ca2+ exchanger superfamily: phylogenetic analysis and structural implications. Mol Biol Evol 21:1692–1703

    Article  PubMed  CAS  Google Scholar 

  • Carafoli E (1991) Calcium pump of the plasma membrane. Physiol Rev 71:129–153

    PubMed  CAS  Google Scholar 

  • Carnelli A, De Michelis MI, Rasi-Caldogno F (1992) Plasma-membrane Ca2+-ATPase of radish seedlings.1. Biochemical-characterization using ITP as a substrate. Plant Physiol 98:1196–1201

    Article  PubMed  CAS  Google Scholar 

  • Case RM, Eisner D, Gurney A, Jones O, Muallem S, Verkhratsky A (2007) Evolution of calcium homeostasis: from birth of the first cell to an omnipresent signalling system. Cell Calcium 42:345–350

    Article  PubMed  CAS  Google Scholar 

  • Catalá R, Santos E, Alonso JM, Ecker JR, Martínez-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

    Article  PubMed  CAS  Google Scholar 

  • Cerana M, Bonza MC, Harris R, Sanders D, De Michelis MI (2006) Abscisic acid stimulates the expression of two isoforms of plasma membrane Ca2+-ATPase in Arabidopsis thaliana seedlings. Plant Biol 8:572–578

    Article  PubMed  CAS  Google Scholar 

  • Chen XF, Chang MC, Wang BY, Wu R (1997) Cloning of a Ca2+-ATPase gene and the role of cytosolic Ca2+ in the gibberellin-dependent signaling pathway in aleurone cells. Plant J 11:363–371

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cheng NH, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347–364

    Article  PubMed  CAS  Google Scholar 

  • Cheng NH, Liu JZ, Nelson RS, Hirschi KD (2004a) Characterization of CXIP4, a novel Arabidopsis protein that activates the H+/Ca2+ antiporter, CAX1. FEBS Lett 559:99–106

    Article  PubMed  CAS  Google Scholar 

  • Cheng NH, Pittman JK, Zhu JK, Hirschi KD (2004b) The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem 279:2922–2926

    Article  PubMed  CAS  Google Scholar 

  • Cheng NH, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138:2048–2060

    Article  PubMed  CAS  Google Scholar 

  • Chung WS, Lee SH, Kim JC, Heo WD, Kim MC, Park CY, Park HC, Lim CO, Kim WB, Harper JF, Cho MJ (2000) Identification of a calmodulin-regulated soybean Ca2+-ATPase (SCA1) that is located in the plasma membrane. Plant Cell 12:1393–1407

    PubMed  CAS  Google Scholar 

  • Corradi GR, Adamo HP (2007) Intramolecular fluorescence resonance energy transfer between fused autofluorescent proteins reveals rearrangements of the N- and C-terminal segments of the plasma membrane Ca2+ pump involved in the activation. J Biol Chem 282:35440–35448

    Article  PubMed  CAS  Google Scholar 

  • Curran AC, Hwang I, Corbin J, Martinez S, Rayle D, Sze H, Harper JF (2000) Autoinhibition of a calmodulin-dependent calcium pump involves a structure in the stalk that connects the transmembrane domain to the ATPase catalytic domain. J Biol Chem 275:30301–30308

    Article  PubMed  CAS  Google Scholar 

  • Dainese P, James P, Baldan B, Carafoli E (1997) Subcellular and tissue distribution, partial purification, and sequencing of calmodulin-stimulated Ca2+-transporting ATPases from barley (Hordeum vulgare L) and tobacco (Nicotiana tabacum). Eur J Biochem 244:31–38

    Article  PubMed  CAS  Google Scholar 

  • De Michelis MI, Carnelli A, Rasi-Caldogno F (1993) The Ca2+ pump of the plasma-membrane of Arabidopsis thaliana – characteristics and sensitivity to fluorescein derivatives. Bot Acta 106:20–25

    Google Scholar 

  • Dieter P, Marmè D (1981) A calmodulin dependent microsomal ATPase from corn (Zea mays L.). FEBS Lett 125:245–248

    Article  CAS  Google Scholar 

  • Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620

    Article  PubMed  CAS  Google Scholar 

  • Downie L, Priddle J, Hawes C, Evans DE (1998) A calcium pump at the higher plant nuclear envelope? FEBS Lett 429:44–48

    Article  PubMed  CAS  Google Scholar 

  • Dunkley TPJ, Hester S, Shadforth IP, Runions J, Weimar T, Hanton SL, Griffin JL, Bessant C, Brandizzi F, Hawes C, Watson RB, Dupree P, Lilley KS (2006) Mapping the Arabidopsis organelle proteome. Proc Natl Acad Sci USA 103:6518–6523

    Article  PubMed  CAS  Google Scholar 

  • DuPont FM, Bush DS, Windle JJ, Jones RL (1990) Calcium and proton transport in membrane-vesicles from barley roots. Plant Physiol 94:179–188

    Article  PubMed  CAS  Google Scholar 

  • Edmond C, Shigaki T, Ewert S, Nelson M, Connorton J, Chalova V, Noordally Z, Pittman JK (2009) Comparative analysis of CAX2-like cation transporters indicates functional and regulatory diversity. Biochem J 418:145–154

    Article  PubMed  CAS  Google Scholar 

  • Ettinger WF, Clear AM, Fanning KJ, Peck ML (1999) Identification of a Ca2+/H+ antiport in the plant chloroplast thylakoid membrane. Plant Physiol 119:1379–1385

    Article  PubMed  CAS  Google Scholar 

  • Evans DE, Williams LE (1998) P-type calcium ATPases in higher plants – biochemical, molecular and functional properties. Biochim Biophys Acta 1376:1–25

    Article  PubMed  CAS  Google Scholar 

  • Evans NH, McAinsh MR, Hetherington AM, Knight MR (2005) ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J 41:615–626

    Article  PubMed  CAS  Google Scholar 

  • Felle HH, Tretyn A, Wagner G (1992) The role of the plasma-membrane Ca2+-ATPase in Ca2+ homeostasis in Sinapis alba root hairs. Planta 188:306–313

    Article  CAS  Google Scholar 

  • Ferrol N, Bennett AB (1996) A single gene may encode differentially localized Ca2+-ATPases in tomato. Plant Cell 8:1159–1169

    PubMed  CAS  Google Scholar 

  • Fusca T, Bonza MC, Luoni L, Meneghelli S, Marrano CA, De Michelis MI (2009) Single point mutations in the small cytoplasmic loop of ACA8, a plasma membrane Ca2+-ATPase of Arabidopsis thaliana, generate partially deregulated pumps. J Biol Chem 284:30881–30888

    Article  PubMed  CAS  Google Scholar 

  • Garciadeblas B, Benito B, Rodriguez-Navarro A (2001) Plant cells express several stress calcium ATPases but apparently no sodium ATPase. Plant Soil 235:181–192

    Article  CAS  Google Scholar 

  • Gaxiola RA, Li JS, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449

    Article  PubMed  CAS  Google Scholar 

  • Geisler M, Axelsen KB, Harper JF, Palmgren MG (2000a) Molecular aspects of higher plant P-type Ca2+-ATPases. Biochim Biophys Acta 1465:52–78

    Article  PubMed  CAS  Google Scholar 

  • Geisler M, Frangne N, Gomès E, Martinoia E, Palmgren MG (2000b) The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol 124:1814–1827

    Article  PubMed  CAS  Google Scholar 

  • George L, Romanowsky SM, Harper JF, Sharrock RA (2008) The ACA10 Ca2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol 146:716–728

    Article  PubMed  CAS  Google Scholar 

  • Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23:441–450

    Article  PubMed  CAS  Google Scholar 

  • Gross J, Marmè D (1978) ATP-dependent Ca2+-uptake into plant membrane vesicles. Proc Natl Acad Sci USA 75:1232–1236

    Article  PubMed  CAS  Google Scholar 

  • Harper JF, Hong BM, Hwang ID, Guo HQ, Stoddard R, Huang JF, Palmgren MG, Sze H (1998) A novel calmodulin-regulated Ca2+-ATPase (ACA2) from Arabidopsis with an N-terminal autoinhibitory domain. J Biol Chem 273:1099–1106

    Article  PubMed  CAS  Google Scholar 

  • Harrar Y, Bellini C, Faure JD (2001) FKBPs: at the crossroads of folding and transduction. Trends Plant Sci 6:426–431

    Article  PubMed  CAS  Google Scholar 

  • Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401–427

    Article  PubMed  CAS  Google Scholar 

  • Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122

    PubMed  CAS  Google Scholar 

  • Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133

    Article  PubMed  CAS  Google Scholar 

  • Hong BM, Ichida A, Wang YW, Gens JS, Pickard BC, Harper JF (1999) Identification of a calmodulin-regulated Ca2+-ATPase in the endoplasmic reticulum. Plant Physiol 119:1165–1175

    Article  PubMed  CAS  Google Scholar 

  • Huang LQ, Berkelman T, Franklin AE, Hoffman NE (1993) Characterization of a gene encoding a Ca2+-ATPase-like protein in the plastid envelope. Proc Natl Acad Sci USA 90:10066–10070

    Article  PubMed  CAS  Google Scholar 

  • Huang LQ, Berkelman T, Franklin AE, Hoffman NE (1994) Errata corrige. Proc Natl Acad Sci USA 91:9664

    Article  CAS  Google Scholar 

  • Hwang I, Ratterman DM, Sze H (1997) Distinction between endoplasmic reticulum-type and plasma membrane-type Ca2+ pumps. Plant Physiol 113:535–548

    Article  PubMed  CAS  Google Scholar 

  • Hwang I, Harper JF, Liang F, Sze H (2000a) Calmodulin activation of an endoplasmic reticulum-located calcium pump involves an interaction with the N-terminal autoinhibitory domain. Plant Physiol 122:157–167

    Article  PubMed  CAS  Google Scholar 

  • Hwang I, Sze H, Harper JF (2000b) A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc Natl Acad Sci USA 97:6224–6229

    Article  PubMed  CAS  Google Scholar 

  • Johnson NA, Liu FL, Weeks PD, Hentzen AE, Kruse HP, Parker JJ, Laursen M, Nissen P, Costa CJ, Gatto C (2009) A tomato ER-type Ca2+-ATPase, LCA1, has a low thapsigargin-sensitivity and can transport manganese. Arch Biochem Biophys 481:157–168

    Article  PubMed  CAS  Google Scholar 

  • Kabala K, Klobus GY (2005) Plant Ca2+-ATPases. Acta Physiol Plant 27:559–574

    Article  CAS  Google Scholar 

  • Kamiya T, Maeshima M (2004) Residues in internal repeats of the rice cation/H+ exchanger are involved in the transport and selection of cations. J Biol Chem 279:812–819

    Article  PubMed  CAS  Google Scholar 

  • Kamiya T, Akahori T, Maeshima M (2005) Expression profile of the genes for rice cation/H+ exchanger family and functional analysis in yeast. Plant Cell Physiol 46:1735–1740

    Article  PubMed  CAS  Google Scholar 

  • 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 Membr Biol 114:133–142

    Article  PubMed  CAS  Google Scholar 

  • Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23:267–278

    Article  PubMed  CAS  Google Scholar 

  • Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489–503

    PubMed  CAS  Google Scholar 

  • Krebs M, Beyhl D, Gorlich E, Al-Rasheid KAS, Marten I, Stierhof Y-D, Hedrich R, Schumacher K (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci USA 107:3251–3256

    Article  PubMed  CAS  Google Scholar 

  • Kurosaki F, Kaburaki H (1994) Calmodulin-dependency of a Ca2+-pump at the plasma membrane of cultured carrot cells. Plant Sci 104:23–30

    Article  CAS  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    Article  PubMed  CAS  Google Scholar 

  • Lapinskas PJ, Cunningham KW, Liu XF, Fink GR, Culotta C (1995) Mutations in PMR1 suppress oxidative damage in yeast-cells lacking superoxide-dismutase. Mol Cell Biol 15:1382–1388

    PubMed  CAS  Google Scholar 

  • Lee SH, Johnson JD, Walsh MP, Van Lierop JE, Sutherland C, Xu AD, Snedden WA, Kosk-Kosicka D, Fromm H, Narayanan N, Cho MJ (2000) Differential regulation of Ca2+/calmodulin-dependent enzymes by plant calmodulin isoforms and free Ca2+ concentration. Biochem J 350:299–306

    Article  PubMed  CAS  Google Scholar 

  • Lee SM, Kim HS, Han HJ, Moon BC, Kim CY, Harper JF, Chung WS (2007) Identification of a calmodulin-regulated autoinhibited Ca2+-ATPase (ACA11) that is localized to vacuole membranes in Arabidopsis. FEBS Lett 581:3943–3949

    Article  PubMed  CAS  Google Scholar 

  • Li X, Chanroj S, Wu Z, Romanowsky SM, Harper JF, Sze H (2008) A distinct endosomalCa2+/Mn2+ pump affects root growth through the secretory process. Plant Physiol 147: 1675–1689

    Article  PubMed  CAS  Google Scholar 

  • Liang F, Sze H (1998) A high-affinity Ca2+ pump, ECA1, from the endoplasmic reticulum is inhibited by cyclopiazonic acid but not by thapsigargin. Plant Physiol 118:817–825

    Article  PubMed  CAS  Google Scholar 

  • Liang F, Cunningham KW, Harper JF, Sze H (1997) ECA1 complements yeast mutants defective in Ca2+ pumps and encodes an endoplasmic reticulum-type Ca2+-ATPase in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:8579–8584

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Zhang XX, Takano T, Liu SK (2009) Characterization of a PutCAX1 gene from Puccinellia tenuiflora that confers Ca2+ and Ba2+ tolerance in yeast. Biochem Biophys Res Commun 383:392–396

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 calmodulin-affinity purification. FEBS Lett 482:225–230

    Article  PubMed  CAS  Google Scholar 

  • Luoni L, Meneghelli S, Bonza MC, De Michelis MI (2004) Auto-inhibition of Arabidopsis thaliana plasma membrane Ca2+-ATPase involves an interaction of the N-terminus with the small cytoplasmic loop. FEBS Lett 574:20–24

    Article  PubMed  CAS  Google Scholar 

  • Luoni L, Bonza MC, De Michelis MI (2006) Calmodulin/Ca2+-ATPase interaction at the Arabidopsis thaliana plasma membrane is dependent on calmodulin isoform showing isoform-specific Ca2+ dependencies. Physiol Plant 126:175–186

    Article  CAS  Google Scholar 

  • Malmström S, Askerlund P, Palmgren MG (1997) A calmodulin-stimulated Ca2+-ATPase from plant vacuolar membranes with a putative regulatory domain at its N-terminus. FEBS Lett 400:324–328

    Article  PubMed  Google Scholar 

  • Malmström S, Åkerlund HE, Askerlund P (2000) Regulatory role of the N terminus of the vacuolar calcium-ATPase in cauliflower. Plant Physiol 122:517–526

    Article  PubMed  Google Scholar 

  • McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294

    Article  PubMed  CAS  Google Scholar 

  • Mei H, Zhao J, Pittman JK, Lachmansingh J, Park S, Hirschi KD (2007) In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Bot 58:3419–3427

    Article  PubMed  CAS  Google Scholar 

  • Mei H, Cheng NH, Zhao J, Park P, Escareno RA, Pittman JK, Hirschi KD (2009) Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4. New Phytol 183:95–105

    Article  PubMed  CAS  Google Scholar 

  • Meneghelli S, Fusca T, Luoni L, De Michelis MI (2008) Dual mechanism of activation of plant plasma membrane Ca2+-ATPase by acidic phospholipids: evidence for a phospholipid binding site which overlaps the calmodulin-binding site. Mol Membr Biol 25:539–546

    Article  PubMed  CAS  Google Scholar 

  • Mills RF, Doherty ML, López-Marqués RL, Weimar T, Dupree P, Palmgren MG, Pittman JK, Williams LE (2008) ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol 146:116–128

    Article  PubMed  CAS  Google Scholar 

  • Miseta A, Kellermayer R, Aiello DP, Fu LW, Bedwell DM (1999) The vacuolar Ca2+/H+ exchanger Vcx1p/Hum1p tightly controls cytosolic Ca2+ levels in S. cerevisiae. FEBS Lett 451:132–136

    Article  PubMed  CAS  Google Scholar 

  • Miwa H, Sun J, Oldroyd GED, Downie JA (2006) Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. Plant J 48:883–894

    Article  PubMed  CAS  Google Scholar 

  • Møller JV, Juul B, le Maire M (1996) Structural organization, ion transport, and energy transduction of P-type ATPases. Biochim Biophys Acta 1286:1–51

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Obara K, Miyashita N, Xu C, Toyoshima L, Sugita Y, Inesi G, Toyoshima C (2005) Structural role of countertransport revealed in Ca2+ pump crystal structure in the absence of Ca2+. Proc Natl Acad Sci USA 102:14489–14496

    Article  PubMed  CAS  Google Scholar 

  • Olbe M, Sommarin M (1998) The spinach plasma membrane Ca2+ pump is a 120-kDa polypeptide regulated by calmodulin-binding to a terminal region. Physiol Plant 103:35–44

    Article  CAS  Google Scholar 

  • Olbe M, Widell S, Sommarin M (1997) Active calcium transporters in isolated membranes of wheat root cells. J Exp Bot 48:1767–1777

    CAS  Google Scholar 

  • Ordenes VR, Reyes FC, Wolff D, Orellana A (2002) A thapsigargin-sensitive Ca2+ pump is present in the pea Golgi apparatus membrane. Plant Physiol 129:1820–1828

    Article  PubMed  CAS  Google Scholar 

  • Palmgren MG, Axelsen KB (1998) Evolution of P-type ATPases. Biochim Biophys Acta 1365:37–45

    Article  PubMed  CAS  Google Scholar 

  • Park S, Cheng NH, Pittman JK, Yoo KS, Park J, Smith RH, Hirschi KD (2005) Increased calcium levels and prolonged shelf life in tomatoes expressing Arabidopsis H+/Ca2+ transporters. Plant Physiol 139:1194–1206

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pittman JK, Mills RF, O'Connor CD, Williams LE (1999) Two additional type IIA Ca2+-ATPases are expressed in Arabidopsis thaliana: evidence that type IIA sub-groups exist. Gene 236:137–147

    Article  PubMed  CAS  Google Scholar 

  • Pittman JK, Shigaki T, Cheng NH, Hirschi KD (2002a) Mechanism of N-terminal autoinhibition in the Arabidopsis Ca2+/H+ antiporter CAX1. J Biol Chem 277:26452–26459

    Article  PubMed  CAS  Google Scholar 

  • Pittman JK, Sreevidya CS, Shigaki T, Ueoka-Nakanishi H, Hirschi KD (2002b) Distinct N-terminal regulatory domains of Ca2+/H+ antiporters. Plant Physiol 130:1054–1062

    Article  PubMed  CAS  Google Scholar 

  • Pittman JK, Shigaki T, Marshall JL, Morris JL, Cheng NH, Hirschi KD (2004) Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter. Plant Mol Biol 56:959–971

    Article  PubMed  CAS  Google Scholar 

  • Pittman JK, Shigaki T, Hirschi KD (2005) Evidence of differential pH regulation of the Arabidopsis vacuolar Ca2+/H+ antiporters CAX1 and CAX2. FEBS Lett 579:2648–2656

    Article  PubMed  CAS  Google Scholar 

  • Pittman JK, Edmond C, Sunderland PA, Bray CM (2009) A cation-regulated and proton gradient-dependent cation transporter from Chlamydomonas reinhardtii has a role in calcium and sodium homeostasis. J Biol Chem 284:525–533

    Article  PubMed  CAS  Google Scholar 

  • Puhakainen T, Pihakaski-Maunsbach K, Widell S, Sommarin M (1999) Cold acclimation enhances the activity of plasma membrane Ca2+ ATPase in winter rye leaves. Plant Physiol Biochem 37:231–239

    Article  CAS  Google Scholar 

  • Qudeimat E, Faltusz AMC, Wheeler G, Lang D, Brownlee C, Reski R, Frank W (2008) A P-IIB-type Ca2+-ATPase is essential for stress adaptation in Physcomitrella patens. Proc Natl Acad Sci USA 105:19555–19560

    Article  PubMed  CAS  Google Scholar 

  • Rasi-Caldogno F, Pugliarello MC, De Michelis MI (1987) The Ca2+-transport ATPase of plant plasma membrane catalyzes a nH+/Ca2+ exchange. Plant Physiol 83:994–1000

    Article  PubMed  CAS  Google Scholar 

  • Rasi-Caldogno F, Carnelli A, De Michelis MI (1993) Controlled proteolysis activates the plasma-membrane Ca2+ pump of higher-plants - a comparison with the effect of calmodulin in plasma-membrane from radish seedlings. Plant Physiol 103:385–390

    PubMed  CAS  Google Scholar 

  • Rasi-Caldogno F, Carnelli A, De Michelis MI (1995) Identification of the plasma membrane Ca2+-ATPase and of its autoinhibitory domain. Plant Physiol 108:105–113

    PubMed  CAS  Google Scholar 

  • Robinson C, Larsson C, Buckhout TJ (1988) Identification of a calmodulin stimulated (Ca2+ + Mg2+) ATPase in a plasma membrane fraction isolated from maize (Zea mays). Physiol Plant 72:177–184

    Article  CAS  Google Scholar 

  • Roh MH, Shingles R, Cleveland MJ, McCarty RE (1998) Direct measurement of calcium transport across chloroplast inner-envelope vesicles. Plant Physiol 118:1447–1454

    Article  PubMed  CAS  Google Scholar 

  • Romani G, Bonza MC, Filippini I, Cerana M, Beffagna N, De Michelis MI (2004) Involvement of the plasma membrane Ca2+-ATPase in the short-term response of Arabidopsis thaliana cultured cells to oligogalacturonides. Plant Biol 6:192–200

    Article  PubMed  CAS  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417

    PubMed  CAS  Google Scholar 

  • Schiøtt M, Palmgren MG (2005) Two plant Ca2+ pumps expressed in stomatal guard cells show opposite expression patterns during cold stress. Physiol Plant 124:278–283

    Article  CAS  Google Scholar 

  • Schiøtt 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

    Article  PubMed  Google Scholar 

  • Schumaker KS, Sze H (1985) A Ca2+/H+ antiport system driven by the proton electrochemical gradient of a tonoplast H+-ATPase from oat roots. Plant Physiol 79:1111–1117

    Article  PubMed  CAS  Google Scholar 

  • Schumaker KS, Sze H (1990) Solubilization and reconstitution of the oat root vacuolar H+/Ca2+ exchanger. Plant Physiol 92:340–345

    Article  PubMed  CAS  Google Scholar 

  • Segarra VA, Thomas L (2008) Topology mapping of the vacuolar Vcx1p Ca2+/H+ exchanger from Saccharomyces cerevisiae. Biochem J 414:133–141

    Article  PubMed  CAS  Google Scholar 

  • Shigaki T, Hirschi KD (2006) Diverse functions and molecular properties emerging for CAX cation/H+ exchangers in plants. Plant Biol 8:419–429

    Article  PubMed  CAS  Google Scholar 

  • Shigaki T, Cheng NH, Pittman JK, Hirschi K (2001) Structural determinants of Ca2+ transport in the Arabidopsis H+/Ca2+ antiporter CAX1. J Biol Chem 276:43152–43159

    Article  PubMed  CAS  Google Scholar 

  • Shigaki T, Barkla BJ, Miranda-Vergara MC, Zhao J, Pantoja O, Hirschi KD (2005) Identification of a crucial histidine involved in metal transport activity in the Arabidopsis cation/H+ exchanger CAX1. J Biol Chem 280:30136–30142

    Article  PubMed  CAS  Google Scholar 

  • Shigaki T, Rees I, Nakhleh L, Hirschi KD (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815–825

    Article  PubMed  CAS  Google Scholar 

  • Snedden WA, Fromm H (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci 3:299–304

    Article  Google Scholar 

  • Subbaiah CC, Sachs MM (2000) Maize cap1 encodes a novel SERCA-type calcium-ATPase with a calmodulin-binding domain. J Biol Chem 275:21678–21687

    Article  PubMed  CAS  Google Scholar 

  • Sze H, Liang F, Hwang I, Curran AC, Harper JF (2000) Diversity and regulation of plant Ca2+ pumps: Insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51:433–462

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ueoka-Nakanishi H, Tsuchiya T, Sasaki M, Nakanishi Y, Cunningham KW, Maeshima M (2000) Functional expression of mung bean Ca2+/H+ antiporter in yeast and its intracellular localization in the hypocotyl and tobacco cells. Eur J Biochem 267:3090–3098

    Article  PubMed  CAS  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  PubMed  CAS  Google Scholar 

  • Williams LE, Schueler SB, Briskin DP (1990) Further characterization of the red beet plasma-membrane Ca2+-ATPase using GTP as an alternative substrate. Plant Physiol 92:747–754

    Article  PubMed  CAS  Google Scholar 

  • Wu ZY, Liang F, Hong BM, Young JC, Sussman MR, Harper JF, Sze H (2002) An endoplasmic reticulum-bound Ca2+/Mn2+ pump, ECA1, supports plant growth and confers tolerance to Mn2+ stress. Plant Physiol 130:128–137

    Article  PubMed  CAS  Google Scholar 

  • Yamniuk AP, Vogel HJ (2004) Structurally homologous binding of plant calmodulin isoforms to the calmodulin-binding domain of vacuolar calcium-ATPase. J Biol Chem 279:7698–7707

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Lavery L, Gill U, Gill K, Steffenson B, Yan GP, Chen XM, Kleinhofs A (2009) A cation/proton-exchanging protein is a candidate for the barley NecS1 gene controlling necrosis and enhanced defense response to stem rust. Theor Appl Genet 118:385–397

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Barkla BJ, Marshall J, Pittman JK, Hirschi KD (2008) The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659–669

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Connorton JM, Guo YQ, Li XK, Shigaki T, Hirschi KD, Pittman JK (2009a) Functional Studies of Split Arabidopsis Ca2+/H+ Exchangers. J Biol Chem 284:34075–34083

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Shigaki T, Mei H, Guo YQ, Cheng NH, Hirschi KD (2009b) Interaction between Arabidopsis Ca2+/H+ Exchangers CAX1 and CAX3. J Biol Chem 284:4605–4615

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  PubMed  CAS  Google Scholar 

  • Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 49:697–725

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Jim Connorton (University of Manchester) for comments to the manuscript and are very grateful to Bob Sharrock (Montana State University) for providing the cif1 picture.

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Correspondence to Jon K. Pittman .

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Pittman, J.K., Bonza, M.C., De Michelis, M.I. (2011). Ca2+ Pumps and Ca2+ Antiporters in Plant Development. In: Geisler, M., Venema, K. (eds) Transporters and Pumps in Plant Signaling. Signaling and Communication in Plants, vol 7. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14369-4_5

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