Abstract
The plasma membrane separates the cellular contents from the surrounding environment. Nutrients must enter through the plasma membrane in order to reach the cell interior, and toxic metabolites and several ions leave the cell by traveling across the same barrier. Biological pumps in the plasma membrane include ABC transporters, vacuolar (V-type) H+ pumps, and P-type pumps. These pumps all utilize ATP as a fuel for energizing pumping. This review focuses on the physiological roles of plasma membrane P-type pumps, as they represent the major ATP hydrolytic activity in this membrane.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alves G, Ameglio T, Guilliot A, Fleurat-Lessard P, Lacointe A, Sakr S, Petel G, Julien JL (2004) Winter variation in xylem sap pH of walnut trees: involvement of plasma membrane H+-ATPase of vessel associated cells. Tree Physiol 24:99–105
Arango M, Gevaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216:355–365
Arguello JM, Eren E, Gonzalez-Guerrero M (2007) The structure and function of heavy metal transport P1B-ATPases. Biometals 20:233–248
Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101
Axelsen KB, Palmgren MG (2001) Inventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol 126:696–706
Axelsen KB, Venema K, Jahn T, Baunsgaard L, Palmgren MG (1999) Molecular dissection of the C-terminal regulatory domain of the plant plasma membrane H+-ATPase AHA2: mapping of residues that when altered give rise to an activated enzyme. Biochemistry 38:7227–7234
Baekgaard L, Fuglsang AT, Palmgren MG (2005) Regulation of plant plasma membrane H +- and Ca 2 +-ATPases by terminal domains. J Bioenerg Biomembr 37:369–374
Baekgaard 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
Baunsgaard L, Venema K, Axelsen KB, Villalba JM, Welling A, Wollenweber B, Palmgren MG (1996) Modified plant plasma membrane H+-ATPase with improved transport coupling efficiency identified by mutant selection in yeast. Plant J 10:451–458
Baxter IR, Young JC, Armstrong G, Foster N, Bogenschutz N, Cordova T, Peer WA, Hazen SP, Murphy AS, Harper JF (2005) A plasma membrane H+-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana. Proc Natl Acad Sci USA 102:2649–2654
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 123:1495–1506
Bonza MC, Luoni L, De Michelis MI (2001) Stimulation of plant plasma membrane Ca2 +-ATPase activity by acidic phospholipids. Physiol Plant 112:315–320
Boursiac Y, Harper JF (2007) The origin and function of calmodulin regulated Ca2+ pumps in plants. J Bioenerg Biomembr 39:409–414
Boutry M, Michelet B, Goffeau A (1989) Molecular cloning of a family of plant genes encoding a protein homologous to plasma membrane H+-translocating ATPases. Biochem Biophys Res Commun 162:567–574
Buch-Pedersen MJ, Pedersen BP, Veierskov B, Nissen P, Palmgren MG (2009) Protons and how they are transported by proton pumps. Pflügers Arch 457:573–579
Camoni L, Iori V, Marra M, Aducci P (2000) Phosphorylation-dependent interaction between plant plasma membrane H+-ATPase and 14-3-3 proteins. J Biol Chem 275:9919–9923
Carafoli E, Brini M (2000) Calcium pumps: structural basis for and mechanism of calcium transmembrane transport. Curr Opin Chem Biol 4:152–161
Certal AC, Almeida RB, Carvalho LM, Wong E, Moreno N, Michard E, Carneiro J, Rodriguez-Leon J, Wu H-M, Cheung AY, Feijo JA (2008) Exclusion of a proton ATPase from the apical membrane is associated with cell polarity and tip growth in Nicotiana tabacum pollen tubes. Plant Cell 20:614–634
Crivici A, Ikura M (1995) Molecular and structural basis of target recognition by calmodulin. Annu Rev Biophys Biomol Struct 24:85–116
Duby G, Boutry M (2008) The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Pflügers Arch 457:645–655
Duby G, Poreba W, Piotrowiak D, Bobik K, Derua R, Waelkens E, Boutry M (2009) Activation of plant pasma membrane H+-ATPase by 14-3-3 proteins is negatively controlled by two phosphorylation sites within the H+-ATPase C-terminal region. J Biol Chem 284:4213–4221
Eren E, Arguello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting PIB-type ATPase, is involved in cytoplasmic Zn 2 + homeostasis. Plant Physiol 136:3712–3723
Eren E, Kennedy DC, Maroney MJ, Arguello JM (2006) A novel regulatory metal binding domain is present in the C-terminus of Arabidopsis Zn2+-ATPase HMA2. J Biol Chem 281:33881–33891
Eren E, Gonzalez-Guerrero M, Kaufman BM, Arguello JM (2007) Novel Zn2 + coordination by the regulatory N-terminus metal binding domain of Arabidopsis thaliana Zn2 +-ATPase HMA2. Biochemistry 46:7754–7764
Frick UB, Schaller A (2002) cDNA microarray analysis of fusicoccin-induced changes in gene expression in tomato plants. Planta 216:83–94
Fuglsang AT, Visconti S, Drumm K, Jahn T, Stensballe A, Mattei B, Jensen ON, Aducci P, Palmgren MG (1999) Binding of 14-3-3 protein to the plasma membrane H+-ATPase AHA2 involves the three C-terminal residues Tyr946-Thr-Val and requires phosphorylation of Thr947. J Biol Chem 274:36774–36780
Fuglsang AT, Borch J, Bych K, Jahn TP, Roepstorff P, Palmgren MG (2003) The binding site for regulatory 14-3-3 protein in plant plasma membrane H+-ATPase: Involvement of a region promoting phosphorylation-independent interaction in addition to the phosphorylation-dependent C-terminal end. J Biol Chem 278:42266–42272
Fuglsang AT, Tulinius G, Cui N, Palmgren MG (2006) Protein phosphatase 2A scaffolding subunit A interacts with plasma membrane H+-ATPase C-terminus in the same regions as 14-3-3 protein. Physiol Plant 128:334–340
Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG, Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 Protein. Plant Cell 19:1617–1634
George L, Romanowsky SM, Harper JF, Sharrock RA (2008) The ACA10 Ca 2 +-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol 146:716–728
Gevaudant F, Duby G, von Stedingk E, Zhao R, Morsomme P, Boutry M (2007) Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance. Plant Physiol 144:1763–1776
Glynn IM (2002) A hundred years of sodium pumping. Annu Rev Physiol 64:1–18
Gomes E, Jakobsen MK, Axelsen KB, Geisler M, Palmgren MG (2000) Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases. Plant Cell 12:2441–2453
Goosey L, Sharrock R (2001) The Arabidopsis compact inflorescence genes: phase-specific growth regulation and the determination of inflorescence architecture. Plant J 26:549–559
Guerini D, Zecca-Mazza A, Carafoli E (2000) Single amino acid mutations in transmembrane domain 5 confer to the plasma membrane Ca2 + pump properties typical of the Ca2 + pump of endo(sarco)plasmic reticulum. J Biol Chem 275:31361–31368
Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395
Harper JF, Surowy TK, Sussman MR (1989) Molecular cloning and sequence of cDNA encoding the plasma membrane proton pump (H+-ATPase) of Arabidopsis thaliana. Proc Natl Acad Sci USA 86:1234–1238
Higgins R, Lockwood T, Holley S, Yalamanchili R, Stratmann JW (2007) Changes in extracellular pH are neither required nor sufficient for activation of mitogen-activated protein kinases (MAPKs) in response to systemin and fusicoccin in tomato. Planta 225:1535–1546
Holdaway-Clarke TL, Weddle NM, Kim S, Robi A, Parris C, Kunkel JG, Hepler PK (2003) Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. J Exp Bot 54:65–72
Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339
Jahn TP, Schulz A, Taipalensuu J, Palmgren MG (2002) Post-translational modification of plant plasma membrane H+-ATPase as a requirement for functional complementation of a yeast transport mutant. J Biol Chem 277:6353–6358
Janicka-Russak M, Kabala K, Burzynski M, Klobus G (2008) Response of plasma membrane H+-ATPase to heavy metal stress in Cucumis sativus roots. J Exp Bot 59:3721–3728
Kinoshita T, Shimazaki K (1999) Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18:5548–5558
Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660
Kinoshita T, Shimazaki K (2001) Analysis of the phosphorylation level in guard-cell plasma membrane H+-ATPase in response to fusicoccin. Plant Cell Physiol 42:424–432
Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55:341–372
Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol 7(6):e1000139
Marin-Manzano MC, Rodriguez-Rosales MP, Belver A, Donaire JP, Venema K (2004) Heterologously expressed protein phosphatase calcineurin downregulates plant plasma membrane H+-ATPase activity at the post-translational level. FEBS Lett 576:266–270
Maudoux O, Batoko H, Oecking C, Gevaert K, Vandekerckhove J, Boutry M, Morsomme P (2000) A plant plasma membrane H+-ATPase expressed in yeast is activated by phosphorylation at its penultimate residue and binding of 14-3-3 regulatory proteins in the absence of fusicoccin. J Biol Chem 275:17762–17770
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
Merlot S, Leonhardt N, Fenzi F, Valon C, Costa M, Piette L, Vavasseur A, Genty B, Boivin K, Muller A, Giraudat J, Leung J (2007) Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J 26:3216–3226
Mills RF, Francini A, Ferreira da Rocha PS, Baccarini PJ, Aylett M, Krijger GC, Williams LE (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579:783–791
Mitchell-Olds T (2001) Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol Evol 16:693–700
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
Morsomme P, de Kerchove D’Exaerde A, De Meester S, Thines D, Goffeau A, Boutry M (1996) Single point mutations in various domains of a plant plasma membrane H+-ATPase expressed in Saccharomyces cerevisiae increase H+-pumping and permit yeast growth at low pH. EMBO J 15:5513–5526
Morsomme P, Dambly S, Maudoux O, Boutry M (1998) Single point mutations distributed in 10 soluble and membrane regions of the Nicotiana plumbaginifolia plasma membrane PMA2 H+-ATPase activate the enzyme and modify the structure of the C-terminal region. J Biol Chem 273:34837–34842
Niittyla T, Fuglsang AT, Palmgren MG, Frommer WB, Schulze WX (2007) Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins of Arabidopsis. Mol Cell Proteomics 6:1711–1726
Nuhse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16:2394–2405
Ottmann C, Marco S, Jaspert N, Marcon C, Schauer N, Weyand M, Vandermeeren C, Duby G, Boutry M, Wittinghofer A, Rigaud JL, Oecking C (2007) Structure of a 14-3-3 coordinated hexamer of the plant plasma membrane H+-ATPase by combining X-ray crystallography and electron cryomicroscopy. Mol Cell 25:427–440
Palmgren MG (1991) Regulation of plant plasma membrane H+-ATPase activity. Physiol Plant 83:314–323
Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Phys Plant Mol Biol 52:817–845
Pardo JM, Serrano R (1989) Structure of a plasma membrane H+-ATPase gene from the plant Arabidopsis thaliana. J Biol Chem 264:8557–8562
Pedersen PL, Carafoli E (1987) Ion motive ATPases. Trends Biochem Sci 12:146–150
Pedersen BP, Buch-Pedersen MJ, Morth JP, Palmgren MG, Nissen P (2007) Crystal structure of the plasma membrane proton pump. Nature 450:1111–1114
Pomorski T, Lombardi R, Riezman H, Devaux PF, van Meer G, Holthuis JCM (2003) Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol Biol Cell 14:1240–1254
Poulsen LR, López-Marqués RL, McDowell SC, Okkeri J, Licht D, Schulz A, Pomorski T, Harper JF, Palmgren MG (2008) The Arabidopsis P4-ATPase ALA3 localizes to the Golgi and requires a beta-subunit to function in lipid translocation and secretory vesicle formation. Plant Cell 20:658–676
Qudeimat E, Faltusz AMC, Wheeler G, Lang D, Brownlee C, Reski 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
Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375
Reddy AS (2001) Calcium: silver bullet in signaling. Plant Sci 160:381–404
Robertson WR, Clark K, Young JC, Sussman MR (2004) An Arabidopsis thaliana plasma membrane proton pump is essential for pollen development. Genetics 168:1677–1687
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417
Schaller A, Oecking C (1999) Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263–272
Schiott M, Romanowsky SM, Baekgaard 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
Schumacher K (2006) Endomembrane proton pumps: connecting membrane and vesicle transport. Curr Opin Plant Biol 9:595–600
Serrano R, Kielland-Brandt MC, Fink GR (1986) Yeast plasma membrane ATPase is essential for growth and has homology with (Na+ + K+), K+- and Ca2+-ATPases. Nature 319:689–693
Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress. Up-regulation of transcription, translation, and threonine-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296
Sinclair SA, Sherson SM, Jarvis R, Camakaris J, Cobbett CS (2007) The use of the zinc-fluorophore, Zinpyr-1, in the study of zinc homeostasis in Arabidopsis roots. New Phytol 174:39–45
Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482
Svennelid F, Olsson A, Piotrowski M, Rosenquist M, Ottman C, Larsson C, Oecking C, Sommarin M (1999) Phosphorylation of Thr-948 at the C terminus of the plasma membrane H+-ATPase creates a binding site for the regulatory 14-3-3 Protein. Plant Cell 11:2379–2392
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
Toyoshima C, Nakasako M, Nomura H, Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405:647–655
Ueno K, Kinoshita T, Inoue SI, Emi T, Shimazaki K (2005) Biochemical characterization of plasma membrane H+-ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. Plant Cell Physiol 46:955–963
Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312
Verret F, Gravot A, Auroy P, Preveral S, Forestier C, Vavasseur A, Richaud P (2005) Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 stretch. FEBS Lett 579:1515–1522
Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EJ, Yazaki K, Theodoulou FL (2008) Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159
Verweij W, Spelt C, Di Sansebastiano GP, Vermeer J, Reale L, Ferranti F, Koes R, Quattrocchio F (2008) An H+ P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nat Cell Biol 10:1456–1462
Vitart V, Baxter I, Doerner P, Harper JF (2001) Evidence for a role in growth and salt resistance of a plasma membrane H+-ATPase in the root endodermis. Plant J 27:191–201
White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511
Williams LE, Mills RF (2005) P(1B)-ATPases – an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502
Yap KL, Kim J, Truong K, Sherman M, Yuan T, Ikura M (2000) Calmodulin target database. J Struct Funct Genomics 1:8–14
Young JC, DeWitt ND, Sussman MR (1998) A transgene encoding a plasma membrane H+-ATPase that confers acid resistance in Arabidopsis thaliana seedlings. Genetics 149:501–507
Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase D alpha1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci USA 101:9508–9513
Zhao R, Dielen V, Kinet J-M, Boutry M (2000) Cosuppression of a plasma membrane H+-ATPase isoform impairs sucrose translocation, stomatal opening, plant growth, and male fertility. Plant Cell 12:535–546
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Palmgren, M.G., Bækgaard, L., López-Marqués, R.L., Fuglsang, A.T. (2011). Plasma Membrane ATPases. In: Murphy, A., Schulz, B., Peer, W. (eds) The Plant Plasma Membrane. Plant Cell Monographs, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13431-9_7
Download citation
DOI: https://doi.org/10.1007/978-3-642-13431-9_7
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-13430-2
Online ISBN: 978-3-642-13431-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)