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Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects

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Abstract

This article will cover historical and recent aspects of reactions and mechanisms involved in the auxin-induced signalling cascade that terminates in the dramatic elongation growth of cells and plant organs. Massive evidence has accumulated that the final target of auxin action is the plasma membrane H+-ATPase, which excretes H+ ions into the cell wall compartment and, in an antiport, takes up K+ ions through an inwardly rectifying K+ channel. The auxin-enhanced H+ pumping lowers the cell wall pH, activates pH-sensitive enzymes and proteins within the wall, and initiates cell-wall loosening and extension growth. These processes, induced by auxin or by the "super-auxin" fusicoccin, can be blocked instantly and specifically by a voltage inhibition of the H+-ATPase due to removal of K+ ions or the addition of K+-channel blockers. Vice versa, H+ pumping and growth are immediately switched on by addition of K+ ions. Furthermore, the treatment of segments either with auxin or with fusicoccin (which activates the H+-ATPase irreversibly) or with acid buffers (from outside) causes an identical transformation and degradation pattern of cell wall constituents during cell-wall loosening and growth. These and other results described below are in agreement with the acid-growth theory of elongation growth. However, objections to this theory are also discussed.

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References

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    PubMed  Google Scholar 

  • Ballio A, Chain EB, De Leo P, Erlanger BF, Mauri M, Rouola A (1964) Fusicoccin: a new wilting toxin produced by Fusicoccum amygdali Del. Nature 203:297

    CAS  Google Scholar 

  • Barkley GM, Leopold AC (1973) Comparative effects of hydrogen ions, carbon dioxide, and auxin on pea stem segment elongation. Plant Physiol 52:76–78

    CAS  Google Scholar 

  • Bates GN, Goldsmith MHM (1983) Rapid response of the plasma-membrane potential in oat coleoptiles to auxin and other weak acids. Planta 159:231–237

    CAS  Google Scholar 

  • Baunsgaard L, Fuglsang AT, Jahn T, Korthout HAA, deBoer AH, Palmgren MG (1998) The 14-3-3 proteins associate with the plant plasma membrane H+-ATPase to generate a fusicoccin binding complex and a fusicoccin responsive system. Plant J 13:661–671

    Article  CAS  PubMed  Google Scholar 

  • Becker K, Hedrich R (2002) Channelling auxin action: modulation of ion transport by indole-3-acetic acid. Plant Mol Biol 49:349–356

    Article  CAS  PubMed  Google Scholar 

  • Bennett AB, Spanswick RM (1983) Optical measurements of ΔpH and Δψ in corn root membrane vesicles: kinetic analysis of Cl-effects on a proton-translocating ATPase. J Membr Biol 71:95–107

    CAS  Google Scholar 

  • Bennett AB, O'Neill SD, Spanswick RM (1984) H+-ATPase activity from storage tissue of Beta vulgaris. Identification and characterization of an anion-sensitive H+-ATPase. Plant Physiol 74:538–544

    CAS  Google Scholar 

  • Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann K (1996) Arabidopsis AUX1 gene, a permease-like regulator of root growth. Science 273:948–950

    Google Scholar 

  • Blatt MR, Slayman CL (1987) Role of "active" potassium transport in the regulation of cytoplasmic pH by non animal cells. Proc Natl Acad Sci USA 84:2737–2741

    CAS  PubMed  Google Scholar 

  • Blatt MR, Thiel G (1994) K+ channels of stomatal guard cells: bimodal control of the K+ inward-rectifier evoked by auxin. Plant J 5:55–68

    CAS  PubMed  Google Scholar 

  • Bonner J (1934) The relation of hydrogen ions to the growth rate of the Avena coleoptile. Protoplasma 21:406–423

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bown AW (1985) CO2 and intracellular pH. Plant Cell Environ 8:459–465

    CAS  Google Scholar 

  • Boysen-Jensen P (1913) Über die Leitung des phototropischen Reizes in der Avenakoleoptile. Ber Dtsch Bot Ges 31:559–566

    Google Scholar 

  • Byrne H, Christou NV, Verna DPS, Maclachlan C (1975) Purification and characterization of two cellulases from auxin-treated pea epicotyls. J Biol Chem 250:1012–1018

    CAS  PubMed  Google Scholar 

  • Cholodny NG (1924) Über die hormonale Wirkung der Organspitze bei der geotropischen Krümmung. Ber Dtsch Bot Ges 42:356–362

    Google Scholar 

  • Cholodny NG (1927) Wuchshormone und Tropismen bei den Pflanzen. Biol Zentralbl 47:604–626

    CAS  Google Scholar 

  • Churchill KA, Sze H (1983) Anion-sensitive, H+-pumping ATPase in membrane vesicles from oat roots. Plant Physiol 71:610–617

    CAS  Google Scholar 

  • Claussen M, Lüthen H, Blatt M, Böttger M (1997) Auxin-induced growth and its linkage to potassium channels. Planta 201:227–234

    CAS  Google Scholar 

  • Cleland R (1971) Cell wall extension. Annu Rev Plant Physiol 22:197–222

    Article  CAS  Google Scholar 

  • Cleland RE (1973) Auxin-induced hydrogen ion excretion from Avena coleoptiles. Proc Natl Acad Sci USA 70:3092–3093

    CAS  Google Scholar 

  • Cleland RE (1976a) Kinetics of hormone-induced H+-excretion. Plant Physiol 58:210–213

    CAS  Google Scholar 

  • Cleland RE (1976b) Fusicoccin-induced growth and hydrogen ion excretion of Avena coleoptiles: relation to auxin responses. Planta 128:201–206

    CAS  Google Scholar 

  • Cleland RE, Prins HBA, Harper JR, Higinbotham W (1977) Rapid hormone-induced hyperpolarization of the oat coleoptile transmembrane potential. Plant Physiol 59:395–397

    CAS  Google Scholar 

  • Cline MG, Edgerton M, Rehm MM (1974) Accelerated-endogenous growth in Avena coleoptile segments. Planta 120:213–214

    Google Scholar 

  • Cooke TJ, Poli D, Sztein AE, Cohen JD (2002) Evolutionary patterns in auxin action. Plant Mol Biol 49:319–338

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (1989) Characterization of long-term extension of isolated cell walls from growing cucumber hypocotyls. Planta 177:121–130

    CAS  PubMed  Google Scholar 

  • Cosgrove DJ (1993) How do plant cell wall extend? Plant Physiol 102:1–6

    Google Scholar 

  • Cosgrove DJ (2000) Expansive growth of plant cell wall. Plant Physiol Biochem 38:109–124

    Article  CAS  PubMed  Google Scholar 

  • Darwin C, Darwin F (1881) The power of movement in plants. Appleton-Century, New York

  • Davidson AL (2002) Not just another ABC transporter. Science 296:1036–1040

    Google Scholar 

  • DeVries H (1874) Über die Dehnbarkeit wachsender Sprosse. Arbeiten Bot Inst Würzburg 1:59–545

  • Dolk HE, Thimann KV (1932) Studies on the growth hormone of plants. Proc Natl Acad Sci USA 18:30

    CAS  Google Scholar 

  • Du Pont FM, Bennett AB, Spanswick RM (1982a) Localisation of a proton-translocating ATPase on sucrose gradients. Plant Physiol 70:1115–1119

    Google Scholar 

  • Du Pont FM, Giorgi DL, Spanswick RM (1982b) Characterization of a proton-translocating ATPase in microsomal vesicles from corn roots. Plant Physiol 70:1694–1699

    Google Scholar 

  • Etherton B (1970) Effect of indole-3-acetic acid on membrane potentials of oat coleoptile cells. Plant Physiol 45:527–528

    CAS  Google Scholar 

  • Evans ML (1985) The action of auxin on plant cell elongation. Crit Rev Plant Sci 2:317–365

    CAS  Google Scholar 

  • Evans ML, Schmitt MR (1975) The nature of spontaneous changes in growth rate in isolated coleoptile segments. Plant Physiol 55:757–762

    CAS  Google Scholar 

  • Evans ML, Ray PM, Reinhold L (1971) Induction of coleoptile elongation by carbon dioxide. Plant Physiol 47:335–341

    CAS  Google Scholar 

  • Ewing NN, Bennett AB (1994) Assessment of a number and expression of P-type H+-ATPase genes in tomato. Plant Physiol 106:547–557

    CAS  PubMed  Google Scholar 

  • Felle H (1989) pH as a second messenger in plants. In: Boss WF, Morre DJ (eds) Second messengers in plant growth and development. Liss, New York, pp 145–166

  • Frachisse JM, Johannes E, Felle H (1988) The use of weak acids as physiological tools: a study of the effectsof fatty acids on intracellular pH and electrical plasmalemma properties of Ricia fluitans rhizoid cells. Biochim Biophys Acta 938:199–210

    Article  CAS  Google Scholar 

  • Frias I, Caldeira MT, Perez-Castineira JR, Navarro-Avino JP, Culianzez-Macia Fa, Kuppinger O, Stransky H, Pages M, Hager A, Serrano R (1996) A major isoform of the maize plasma membrane H+-ATPase: characterization and induction by auxin in coleoptiles. Plant Cell 8:1533–1544

    CAS  PubMed  Google Scholar 

  • Friml J, Palme K (2002) Polar auxin transport—old questions and new concepts? Plant Mol Biol 49:237–284

    Google Scholar 

  • Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809

    Google Scholar 

  • Fry SC (1989) Cellulases, hemicellulases and auxin-stimulated growth: a possible relationship. Physiol Plant 75:532–536

    CAS  Google Scholar 

  • Fry SC, Smith RC, Renwick KF, Martin DJ, HodgeSK, Matthews KJ (1992) Xyloglucan endotransglucosylase, a new wall-loosening enzyme activity from plants. Biochem J 282:821–828

    CAS  Google Scholar 

  • Fuglsang AT, Visconti S, Dumm K, Jahn T, Stemballe A, Mattei B, Jensen ON, Palmgren MG (1999) Binding of 14-3-3 protein to the plasma membrane H+-ATPase AMA2 involves the three C-terminal residues Thyr946-Thr-Val and requires phosphorylation of Thr949. J Biol Chem 274:36774–36780

    CAS  PubMed  Google Scholar 

  • Fullone MR, Visconti S, Marra M, Fogliano V, Aducci P (1998) Fusicoccin effect on the in vitro interaction between plant 14-3-3 proteins and plasma membrane H+-ATPase. J Biol Chem 273:7698–7702

    Article  CAS  PubMed  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yepremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230

    PubMed  Google Scholar 

  • Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Google Scholar 

  • Greenwood MS, Shaw S, Hillman JR, Richie A, Wilkins MB (1972) Identification of auxin from Zea coleoptile tips by mass spectrometry. Planta 108:179–183

    CAS  Google Scholar 

  • Guern J, Mathieu Y, Péan M, Pasquier C, Beloeil JC, Lallemand JY (1986) Cytoplasmic pH regulation in Acer Pseudoplatanus cells. I. A31P NMR description of acid-load effect. Plant Physiol 82:840–845

    CAS  Google Scholar 

  • Haagen-Smit AJ, Dandliker WB, Wittwer SH, Murneek AE (1946) Isolation of 3-indolacetic acid from immature corn kernels. Am J Bot 33:118–120

    CAS  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promotors and regulatory factors. Plant Mol Biol 49:373–385

    Article  CAS  PubMed  Google Scholar 

  • Hager A (1955) Chloroplasten-Farbstoffe, ihre papierchromatographische Trennung und ihre Veränderungen durch Außenfaktoren. Z Naturforsch 10B:310–312

    CAS  Google Scholar 

  • Hager A (1962) Untersuchungen über einen durch H+-Ionen induzierbaren Zellstreckungsmechanismus (Analysis of a cell elongation mechanism induced by H+ ions). Habilitationsschrift, Faculty of Natural Sciences, University of Munich, pp 1–54

  • Hager A (1966) Die Zusammenhänge zwischen lichtinduzierten Xanthopyhll-Umwandlungen und Hill-Reaktion. (Correlations between light-induced xanthophyll transformations and Hill-reaction). Ber Dtsch Bot Ges 79:94–107

    CAS  Google Scholar 

  • Hager A (1969) Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin-Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. (Light-dependent decrease of the pH value in a chloroplast compartment causing the enzymatic interconversion of violaxanthin to zeaxanthin; relations to photophosphorylation). Planta 89:224–243

    CAS  Google Scholar 

  • Hager A (1980a) The reversible, light-induced conversions of xanthophylls in the chloroplast. In: Czygan FD (ed) Pigments in plants, 2nd edn. Fischer, Stuttgart, pp 57–79

  • Hager A (1980b) Avena coleoptile segments: hyperelongation growth after anaerobic treatment. Z Naturforsch 35C:794–804

    CAS  Google Scholar 

  • Hager A (1986) Citation classic commentary to "Hager A, Menzel H, Krauss A (1971) Versuche und Hypothese zur Primärwirkung des Auxins beim Streckungswachstum (Experiments and hypothesis concerning the primary action of auxin in elongation growth)". Planta 100:47–75. Also in Current Contents (Life Sciences) (1984) 27(10): 12 and in J. Barrett (ed) Contemporary classics in the life sciences, vol I. Cell biology (1986). ISI, Philadelphia, p 285

    Google Scholar 

  • Hager A (1989) Chloroplast pigment chromatography and xanthophyll cycle. Citation Classic commentary. Current Contents (Life Sciences) 32(10): 15

    Google Scholar 

  • Hager A, Biber W (1984) Functional and regulatory properties of H+-pumps at the tonoplast and plasma membranes of Zea mays coleoptiles. Z Naturforsch 39C:927–937

    CAS  Google Scholar 

  • Hager A, Helmle M (1981) Properties of an ATP-fueled, Cl--dependent proton pump localized in membranes of microsomal vesicles from maize coleoptiles. Z Naturforsch 36C:997–1008

    CAS  Google Scholar 

  • Hager A, Meyer-Bertenrath TH (1966) Die Isolierung und quantitative Bestimmung der Carotinoide und Chlorophylle von Blättern, Algen und isolierten Chloroplasten mit Hilfe dünnschichtchromatographischer Methoden (Extraction and quantitative determination of carotenoids and chlorophylls of leaves, algae and isolated chloroplasts by thin-layer chromatographic techniques. Planta 69:198–217

    CAS  Google Scholar 

  • Hager A, Moser I (1985) Acetic acid esters and permeable weak acids induce active proton extrusion and extension growth of coleoptile segments by lowering the cytoplasmic pH. Planta 163:391–400

    CAS  Google Scholar 

  • Hager A, Menzel H, Krauss A (1971) Versuche und Hypothese zur Primärwirkung des Auxins beim Streckungswachstum (Experiments and hypothesis concerning the primary action of auxin in elongation growth). Planta 100:47–75

    CAS  Google Scholar 

  • Hager A, Frenzel R, Laible D (1980) ATP-dependent proton transport into vesicles of microsomal membranes of Zea mays coleoptiles. Z Naturforsch 35C:783–793

    CAS  Google Scholar 

  • Hager A, Berthold W, Biber W, Edel HG, Lanz Ch, Schiebel G (1986) Primary and secondary energized ion translocating systems on membranes of plant cells. Ber Dtsch Bot Ges 99:281–295

    Google Scholar 

  • Hager A, Brich M, Debus G, Edel HG, Priester TH (1989) Membrane metabolism and growth. Phospholiphases, protein kinases and exocytotic processes in coleoptiles of Zea mays. In: M. Tazawa et al. (eds) Plant water relations and growth under stress. Proceedings of the Yamada Conference XXII, Osaka, Japan. Yamada Science Foundation, Tokyo, pp 275–282

  • Hager A, Debus G, Edel HG, Stransky H, Serrano R (1991) Auxin induces exocytosis and the rapid synthesis of a high-turnover pool of plasma membrane H+-ATPase. Planta 185:527–537

    CAS  Google Scholar 

  • Haschke HP, Lüttge U (1973) β-Indolylessigsäure (IES)-abhängiger K+-H+-Austauschmechanismus und Streckungswachstum bei Avena-Koleoptilen. Z Naturforsch 28C:555–558

    Google Scholar 

  • Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168

    Google Scholar 

  • Hayashi T, Whon YS, Maclachlan G (1984) Pea xyloglucan and cellulose. II. Hydrolysis by pea endo-1,4-β-glucanases. Plant Physiol 75:605–610

    CAS  Google Scholar 

  • Hedrich R, Dietrich P (1996) Plant K+ channels: similarity and diversity. Bot Acta 109:94–101

    CAS  Google Scholar 

  • Hertel R (1983) The mechanism of auxin transport as a model for auxin action. Z Pflanzenphysiol 112:53–67

    CAS  Google Scholar 

  • Hertel R, Thomson KS, Russo V (1972) In vitro auxin binding to particulate cell fractions from corn coleoptiles. Planta 107:325–340

    CAS  Google Scholar 

  • Heyn ANJ (1931) Der Mechanismus der Zellstreckung. Rec Trav Bot Neerl 28:113–244

    Google Scholar 

  • Hodges TK, Leonard RT, Bracker CE, Keenan TW (1972) Purification of an ion-stimulated ATPase from plant roots: association with plasma membranes. Proc Natl Acad Sci USA 69:3307–3311

    CAS  Google Scholar 

  • Hoson T (1998) Apoplast as the site of response to environmental signals. J Plant Res 111:167–177

    CAS  PubMed  Google Scholar 

  • Hoson T, Masuda Y (1991) Inhibition of auxin-induced elongation and xyloglucan breakdown in azuki bean epicotyl segments by fucose-binding lectins. Physiol Plant 82:41–47

    Article  CAS  Google Scholar 

  • Hoson T, Masuda Y, Sone Y, Misaki A (1991) Xyloglucase antibodies inhibit auxin-induced elongation and cell wall loosening of azuki bean epicotyls but not of oat coleoptiles. Plant Physiol 96:551–557

    CAS  Google Scholar 

  • Hoson T, Tabuchi A, Masuda Y (1995) Mechanism of xyloglucan breakdown in cell walls of azuki bean epicotyls. J Plant Physiol 147:219–224

    CAS  Google Scholar 

  • Ikoma S, Okamoto H (1988) The quantitative and chronological relationship between IAA-induced H+ pump activation and elongation growth studied by means of xylem perfusion. Plant Cell Physiol 29:261–267

    CAS  Google Scholar 

  • Jacobs M, Ray PM (1976) Rapid auxin-induced decrease in free space pH and its relationship to auxin-induced growth in maize and pea. Plant Physiol 58:203–209

    CAS  Google Scholar 

  • Jahn T, Johansson F, Lüthen H, Volkmann D, Larsson C (1996) Reinvestigation of auxin and fusicoccin stimulation of the plasma membrane H+-ATPase activity. Planta 199:359–365

    CAS  Google Scholar 

  • Jahn T, Fuglsang AT, Olsson A, Bruntrup IM, Collinge DB, Volkman D, Sommarin M, Palmgren MG, Larsson C (1997) The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H+-ATPase. Plant Cell 9:1805–1814

    CAS  PubMed  Google Scholar 

  • Kaku T, Tabuchi A, Wakabayashi K, Kamisaka S, Hoson T (2002) Action of xyloglucan hydrolase within the native cell wall architecture and its effect on cell wall extensibility in azuki bean epicotyls. Plant Cell Physiol 43:21–26

    CAS  PubMed  Google Scholar 

  • Katou K, Ichino K (1982) Effects of carbon dioxide on the spatially separate electrogenic ion pumps and the growth rate in the hypocotyl of Vigna sesquipedalis. Planta 155:486–492

    CAS  Google Scholar 

  • Katou K, Okamoto H (1970) Distribution of electric potential and ion transport in the hypocotyl of Vigna sesquipedalis. I. Distribution of overall ion concentration and the role of hydrogen ion in generation of potential difference. Plant Cell Physiol 11:385–402

    CAS  Google Scholar 

  • Kerkeb L, Venema K, Donaire JP, Rodríguez-Rosales MP (2002) Enhanced H+/ATP coupling ratio of H+-ATPase and increased14-3-3 protein content in plasma membrane of tomato cell upon osmotic shock. Physiol Plant 116:37–41

    Article  PubMed  Google Scholar 

  • Kim YS, Min JK, Kim D, Jung J (2001) A soluble auxin binding protein, ABP57: purification with anti-bovine serum albumin antibody and characterization of its mechanistic role in auxin effect on plant plasma membrane H+-ATPase. J Biol Chem 276:10730–10736

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kögl F, Haagen-Smit AJ (1931) Über die Chemie des Wuchsstoffs. Proc Kon Akad Wetensch Amsterdam 34:1411–1416

    Google Scholar 

  • Kögl F, Haagen-Smit AJ, Erxleben H (1933) Über ein Phytohormon der Zellstreckung. Reindarstellung des Auxins aus menschlichem Harn. IV. Mitteilung. Z Physiol Chem 220:137–161

    Google Scholar 

  • Kögl F, Haagen-Smit AJ, Erxleben H (1934) Über ein neues Auxin ("Heteroauxin") aus Harn. XI. Mitteilung. Z Physiol Chem 228:90–103

    Google Scholar 

  • Korthout HAAJ, deBoer AH (1994) A fusicoccin binding protein belongs to the family of 14-3-3-brain protein homologs. Plant Cell 6:1681–1692

    Article  CAS  PubMed  Google Scholar 

  • Kotake T, Nakagawa N, Takeda K, Sakurai N (2000) Auxin-induced elongation growth and expressions of cell wall-bound exo-and endo-β-glucanases in barley coleoptiles. Plant Cell Physiol 41:1272–1278

    CAS  PubMed  Google Scholar 

  • Kurkdjian A, Guern J (1989) Intracellular pH: measurement and importance in cell activity. Annu Rev Plant Physiol Plant Mol Biol 40:271–303

    Google Scholar 

  • Kurkdjian A, Leguay JJ, Guern J (1978) Measurement of intracellular pH and aspects of its control in higher plant cells cultivated in liquid medium. Respir Physiol 33:75–89

    Google Scholar 

  • Kutschera U (1990) Cell-wall synthesis and elongation growth in hypocotyls of Helianthus annuus L. Planta 181:316–323

    Google Scholar 

  • Kutschera U (1994) The current status of the acid-growth hypothesis. New Phytol 126:549–569

    CAS  Google Scholar 

  • Kutschera U, Schopfer P (1985) Evidence against the acid growth theory of auxin action. Planta 163:483–493

    CAS  Google Scholar 

  • Labawitch JM, Ray PM (1974) Turnover of cell wall polysaccharides in elongating pea stem segments. Plant Physiol 53:669–673

    CAS  Google Scholar 

  • Lew RR, Spanswick RM (1985) Characterization of anion effects on the nitrate-sensitive ATP-dependent proton pumping activity of soybean (Glycine max L.) seedling root microsomes. Plant Physiol 77:352–357

    CAS  Google Scholar 

  • Li Y, Darley CP, Ongaro V, Fleming A, Schipper O, Baldauf SL, McQueen-Mason SJ (2002) Plant expansins are a complex multigene family with an ancient evolutionary origin. Plant Physiol 128:854–864

    Article  CAS  PubMed  Google Scholar 

  • Löbler M, Klämbt D (1985a) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). I. Purification by immunological methods and characterization. J Biol Chem 260:9848–9853

    PubMed  Google Scholar 

  • Löbler M, Klämbt D (1985b) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). II. Localization of a putative auxin receptor. J Biol Chem 260:9854–9859

    PubMed  Google Scholar 

  • Lorences EP, Zarra J (1987) Auxin-induced growth in hypocotyl segments of Pinus pinaster Aiton—changes in molecular weight distribution of hemicellulosic polysaccharides. J Exp Bot 38:960–967

    CAS  Google Scholar 

  • Lüthen H, Bigdon M, Böttger M (1990) Reexamination of acid growth theory of auxin action. Plant Physiol 93:931–939

    Google Scholar 

  • Lüthen H, Claussen M, Böttger M (1999) Growth: progress in auxin research. In: Progress in Botany, vol 60. Springer, Berlin Heidelberg New York, pp 315–340

  • Lüttge U, Higinbothan N, Pallaghy CK (1972) Electrochemical evidence of specific action of indole acetic acid on membranes of Mnium leaves. Z Naturforsch 27B:1239–1242

    Google Scholar 

  • Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G (2002) AUX 1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in Arabidopsis seedlings. Plant Cell 14:589–597

    Article  CAS  PubMed  Google Scholar 

  • Marra M, Fullone MR, Fogliano V, Pen J, Mattei M, Masi S, Aducci P (1994) The 30-kilodalton protein present in purified fusicoccin receptor preparation is a 14-3-3-like protein. Plant Physiol 106:1497–1501

    Article  CAS  PubMed  Google Scholar 

  • Marrè E (1979) Fusicoccin: a tool in plant physiology. Annu Rev Plant Physiol 30:273–288

    Article  Google Scholar 

  • Marrè E, Lado P, Rasi Caldogno F, Colombo R (1973) Correlation between cell enlargement in pea internode segments and decrease in the pH of the medium of incubation. I. Effects of fusicoccin, natural and synthetic auxins and mannitol. Plant Sci Lett 1:179–184

    Article  Google Scholar 

  • Marrè E, Lado P, Ferroni A, Ballarin-Denti A (1974) Transmembrane potential increase induced by auxin, benzyladenine and fusicoccin. Correlation with proton extrusion and cell enlargement. Plant Sci Lett 2:257–265

    Google Scholar 

  • Matsumoto T, Sakai F, Hayashi T (1997) A xyloglucan-specific endo-1,4-β-glucanase isolated from auxin-treated pea stems. Plant Physiol 114:661–667

    CAS  PubMed  Google Scholar 

  • McClure BA, Hagen G, Brown CS, Gee MA, Guilfoyle TJ (1989) Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean. Plant Cell 1:229–239

    CAS  PubMed  Google Scholar 

  • McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between wall polymers by proteins that induce plant wall extension. Proc Natl Acad Sci USA 91:6574–6578

    CAS  Google Scholar 

  • McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433

    CAS  Google Scholar 

  • Menzel H (1966) Die pH-abhängige Veränderung mechanischer und chemischer Eigenschaften der Zellwand und ihr Zusammenhang mit der Wuchsstoffwirkung. PhD thesis, University of Munich, Germany, pp 1–57

  • Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148

    CAS  Google Scholar 

  • Mizuno A, Katou K (1992) Effect of cations on IAA-induced proton excretion in the xylem of Vigna unguinculata. Physiol Plant 85:411–416

    Article  CAS  Google Scholar 

  • Mizuno A, Kojima H, Katou K, Okamoto H (1985) The electrogenic proton pumping from parenchyma symplast into xylem—direct demonstration by xylem perfusion. Plant Cell Environ 8:525–529

    Google Scholar 

  • Morandini P, Valera M, Albumi C, Bonza MC, Giacometti S, Ravera G, Murgia J, Soave C, DeMichelis MJ (2002) A novel interaction partner for the C-terminus of Arabidopsis thaliana plasma membrane H+-ATPase (AHA1 isoform): site and mechanism of action on H+-ATPase activity differ from those of 14-3-3 proteins. Plant J 31:487–497

    Article  CAS  PubMed  Google Scholar 

  • Morsomme P, de Kerchove d'Exaerde A, De Meester S, Thines D, Goffeau A, Boutry M (1996) Single point mutations in various domains of plant plasma membrane H+-ATPase expressed in S. cerevisiae increase H+-pumping and permit yeast growth at low pH. EMBO J 20:5513–5526

    Google Scholar 

  • Napier RM, Venis MA (1990) Monoclonal antibodies detect an auxin-induced conformational change in the maize auxin-binding protein. Planta 182:313

    CAS  Google Scholar 

  • Napier RM, David KM, Perrot-Rechenmann C (2002) A short history of auxin-binding protein. Plant Mol Biol 49:339–348

    Article  CAS  PubMed  Google Scholar 

  • Nielsen N (1924) Studies on the transmission of stimuli in the coleoptile of Avena. Dansk Bot Ark 4:Nr. 8

  • Nishitani K, Masuda Y (1981) Auxin-induced changes in the cell wall structure: Changes in the sugar composition, intrinsic viscosity and molecular weight distributions of matrix polysaccharides of the epicotyl cell wall of Vigna angularis. Physiol Plant 52:482–494

    CAS  Google Scholar 

  • Nishitani K, Masuda Y (1982) Acid pH-induced structural changes in cell wall xyloglucans in Vigna agularis epicotyl segments. Plant Sci Lett 28:87–94

    CAS  Google Scholar 

  • Nitsch JP, Nitsch C (1956) Studies on the growth of coleoptile and first internode sections. A new, sensitive, straight-growth test for auxins. Plant Physiol 31:94–111

    CAS  Google Scholar 

  • Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis reprised for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454

    CAS  PubMed  Google Scholar 

  • Oecking C, Eckerskorn C, Weiler EW (1994) The fusicoccin receptor of plants is a member of the 14-3-3 superfamily of eukaryotic regulatory proteins. FEBS Lett 352:163–166

    Article  CAS  PubMed  Google Scholar 

  • Oecking C, Piotrowski M, HagemeierJ, Hagemann K (1997) Topology and target interaction of the fusicoccin-binding 14-3-3 homologs of Commelina communis. Plant J 12:441–453

    CAS  Google Scholar 

  • Okamoto H, Okamoto A (1994) The pH-dependent yield threshold of cell wall in a glycerinated hollow cylinder (in vitro system) of cowpea hypocotyl. Plant Cell Environ 17:979–983

    Google Scholar 

  • Okamoto H, Mizuno A, Katou K, Ono Y, Matsumura Y, Kojima H (1984) A new method in growth electro-physiology: pressurized intra-organ perfusion. Plant Cell Environ 7:139–147

    Google Scholar 

  • Okamoto-Nakazato A, Nakamura T, Okamoto H (2000a) The isolation of wall-bound proteins regulating yield threshold tension in glycerinated hollow cylinders of cowpea hypocotyl. Plant Cell Environ 23:145–154

    CAS  Google Scholar 

  • Okamoto-Nakazato A, Takahashi K, Kido N, Owarabi K, Katou K (2000b) Molecular cloning of yieldins regulating the yield threshold of cow pea cell walls: cDNA cloning and characterization of recombinant yieldin. Plant Cell Environ 23:155–164

    CAS  Google Scholar 

  • Okamoto-Nakazato A, Takahashi K, Katoh-Semba R, Katou K (2001) Distribution of yieldin, a regulatory protein of the cell wall yield threshold in etiolated cowpea seelings. Plant Cell Physiol 42:952–958

    CAS  PubMed  Google Scholar 

  • Olsson A, Svennelid F, Ek B, Sommarin M, Larsson C (1998) A phosphothreonine residue at the C-terminal end of the plasma membrane H+-ATPase is protected by fusicoccin-induced 14-3-3 binding. Plant Physiol 118:551–555

    CAS  PubMed  Google Scholar 

  • Paál A (1918) Über phototropische Reizleitung. Jahrb Wiss Bot 58:406–458

    Google Scholar 

  • Palmgren MG (1998) Proton gradients and plant growth: role of the plasma membrane H+-ATPase. Adv Bot Res 28:1–70

    CAS  Google Scholar 

  • Palmgren MG (2001) Plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845

    CAS  PubMed  Google Scholar 

  • Palmgren MG, Sommarin M, Serrano R, Larsson C (1991) Identification of an autoinhibitory domain in the C-terminal region of the plant plasma membrane H+-ATPase. J Biol Chem 266:20470–20475

    CAS  PubMed  Google Scholar 

  • Pardo JM, Serrano R (1989) Structure of a plasma membrane H+-ATPase gene from the plant Arabidopsis thaliana. J Biol Chem 264:8557–8562

    CAS  PubMed  Google Scholar 

  • Philippar K, Fuchs J, Lüthen H, Hoth S, Bauer CS, Haga K, Thiel G, Ljung K, Sandberg G, Böttger M, Becker D, Hedrich R (1999) Auxin-induced K+-channel expression represents an essential step in coleoptile growth and gravitropism. Proc Natl Acad Sci USA 96:12186–12191

    CAS  PubMed  Google Scholar 

  • Piotrowski M, Morsomme P, Boutry M, Oecking C (1998) Complementation of the Sacccharomyces cerevisiae plasma membrane H+-ATPase by a plant H+-ATPase generates a highly abundant fusicoccin binding site. J Biol Chem 273:30018–30023

    Article  CAS  PubMed  Google Scholar 

  • Poole RJ (1978) Energy coupling for membrane transport. Annu Rev Plant Physiol 29:437–460

    Article  CAS  Google Scholar 

  • Prat R (1978) Gradient of growth, spontaneous changes in growth rate and response to auxin of excised hypocotyl segments of Phaseolus aureus. Plant Physiol 62:75–79

    CAS  Google Scholar 

  • Rayle DL (1973) Auxin-induced hydrogen-ion secretion in Avena coleoptiles and its implications. Planta 114:63–73

    CAS  Google Scholar 

  • Rayle DL, Cleland R (1970) Enhancement of wall loosening and elongation by acid solutions. Plant Physiol 46:250–253

    CAS  Google Scholar 

  • Rayle DL, Cleland R (1977) Control of plant cell enlargement by hydrogen ions. Curr Top Dev Biol 11:187–211

    CAS  PubMed  Google Scholar 

  • Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274

    CAS  PubMed  Google Scholar 

  • Rayle DL, Nowbar S, Cleland RE (1991) The epidermis of the pea epicotyl is not a unique target tissue for auxin-induced growth. Plant Physiol 97:449–451

    CAS  PubMed  Google Scholar 

  • Roland JC, Reis D, Mosiniak M, Vian B (1982) Cell wall texture along the growth gradient of mung bean hypocotyl: ordered assembly and dissipative processes. J Cell Sci 56:303–318

    Google Scholar 

  • Romani G, Marrè MT, Bellando M, Alloatti G, Marrè E (1985) H+ extrusion and potassium uptake associated with potential hyperpolarization in maize and wheat root segments treated with permeant weak acids. Plant Physiol 79:734–739

    CAS  Google Scholar 

  • Rück A, Palme K, Venis MA, Napier RM, Felle HM (1993) Patch-clamp analysis establishes a role for an auxin binding protein in the auxin stimulation of plasma membrane current in Zea mays protoplasts. Plant J 4:41–46

    Article  Google Scholar 

  • Ruge U (1937) Untersuchungen über den Einfluß des Heteroauxins auf das Streckungswachstum des Hypokotyls von Helianthus annuus. Z Bot 31:1–56

    CAS  Google Scholar 

  • Sapozhnikov DJ (1969) Transformation of xanthophylls in the chloroplasts. In: Metzner H (ed) Progress in photosynthesis research, vol 2. Kluwer, Dordrecht, pp 694–700

  • Sargent JA, Atack AV, Osborne DJ (1974) Auxin and ethylene control of growth in epidermal cells of Pisum sativum: a biphasic response to auxin. Planta 115:213–225

    CAS  Google Scholar 

  • Scherer GFE (2002) Secondary messengers and phospholipase A2 in auxin signal transduction. Plant Mol Biol 49:357–372

    Article  CAS  PubMed  Google Scholar 

  • Scherer GFE, André B (1989) A rapid response to a plant hormone: auxin stimulates phosphilipase A2 in vivo and in vitro. Biochem Biophys Res Commun 163:111–117

    CAS  PubMed  Google Scholar 

  • Schnepf E, Deichgräber G (1979) Elongation growth of setae of Pellia (Bryophyta): fine structure analysis. Z Pflanzenphysiol 94:283–297

    Google Scholar 

  • Schopfer P (1993) Determination of auxin-dependent pH changes in coleoptile cell walls by a null-point method. Plant Physiol 103:351–357

    CAS  PubMed  Google Scholar 

  • Sergeeva E, Liaimer A, Bergman B (2002) Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215:229–238

    Article  CAS  PubMed  Google Scholar 

  • Serrano R (1984) Purification of the proton pumping ATPase from plant plasma membranes. Biochem Biophys Res Commun 121:735–740

    CAS  PubMed  Google Scholar 

  • Serrano R (1989) Structure and function of plasma membrane ATPase. Annu Rev Plant Physiol Plant Mol Biol 40:61–94

    Google Scholar 

  • Slayman CL, Long WS, Lu CYH (1973) The relationship between ATP and an electrogenic pump in the plasma membrane of Neurospora crassa. J Membr Biol 14:305–338

    CAS  PubMed  Google Scholar 

  • Söding H (1923) Werden von der Spitze der Haferkoleoptile Wuchshormone gebildet? Ber Dtsch Bot Ges 41:396–400

    Google Scholar 

  • Söding H (1925) Zur Kenntnis der Wuchshormone in der Haferkoleoptile. Jahrb Wiss Bot 64:587–603

    Google Scholar 

  • Söding H (1931) Wachstum und Wanddehnbarkeit bei der Haferkoleoptile. Jahrb Wiss Bot 74:127–151

    Google Scholar 

  • Soga K, Wakabayashi K, Hoson T, Kamisaka S (2000) Flower stalk segments of Arabidopsis thaliana ecotype Columbia lack the capacity to grow in response to exogenously applied auxin. Plant Cell Physiol 41:1327–1333

    Article  CAS  PubMed  Google Scholar 

  • Spanswick RM (1981) Electrogenic ion pumps. Annu Rev Plant Physiol 32:267–289

    Article  CAS  Google Scholar 

  • Squire GR, Mansfield TA (1972) Studies of the mechanism of action of fusicoccin, the fungal toxin that induces wilting, and its interaction with abscisic acid. Planta 105:71–78

    CAS  Google Scholar 

  • Stark P (1921) Studien über traumatotrope und haptotrope Reizleitungsvorgänge. Jb Wiss Bot 60:67–134

    Google Scholar 

  • Starrach N, Mayer WE (1986) Unequal distribution of fixed negative charges in isolated cell walls of various tissues in primary leaves of Phaseolus. J Plant Physiol 126:213–222

    CAS  Google Scholar 

  • Starrach N, Mayer WE (1989) Changes of the apoplastic pH and K+ concentration in the Phaseolus pulvinus in situ in relation to rhythmic leaf movements. J Exp Bot 40:865–873

    CAS  Google Scholar 

  • Starrach N, Flach D, Mayer WE (1985) Activity of fixed negative charges of isolated extensor cell walls of the laminar pulvinus of primary leaves of Phaseolus. J Plant Physiol 120:441–455

    CAS  Google Scholar 

  • Steffens B, Feckler C, Palme K, Christian M, Böttger M, Lüthen H (2001) The auxin signal for protoplast swelling is perceived by extracellular ABP1. Plant J 27:591–599

    PubMed  Google Scholar 

  • Stout RG, Cleland RE (1982) Evidence for a Cl--stimulated Mg ATPase proton pump in oat root membranes. Plant Physiol 69:798–803

    CAS  Google Scholar 

  • Strugger S (1932) Die Beeinflussung des Wachstums und des Geotropismus durch die Wasserstoffionen. Ber Dtsch Bot Ges 50[Appendix]:77–92

  • Sussman MR (1994) Molecular analysis of proteins in the plant plasma membrane. Annu Rev Plant Physiol Plant Mol Biol 45:211–234

    CAS  Google Scholar 

  • 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 11:2379–2391

    CAS  PubMed  Google Scholar 

  • Sze H (1980) Nigericin-stimulated ATPase activity in microsomal vesicles of tobacco callus. Proc Natl Acad Sci USA 77:5904–5908

    CAS  Google Scholar 

  • Sze H (1985) H+-translocating ATPases: Advances using membrane vesicles. Annu Rev Plant Physiol 36:175–208

    CAS  Google Scholar 

  • Sze H, Li X, Palmgren MG (1999) Energization of plant cell membranes by H+-pumping ATPases: regulation and biosynthesis. Plant Cell 11:677–689

    Article  CAS  PubMed  Google Scholar 

  • Tabuchi A, Kamisaka S, Hoson T (1997) Purification of xyloglucan hydrolase/endotransferase from cell walls of azuki bean epicotyls. Plant Cell Physiol 38:653–658

    CAS  Google Scholar 

  • Tabuchi A, Mori H, Kamisaka S, Hoson T (2001) A new type of endo-xyloglucan transferase devoted to xyloglucan hydrolysis in the cell wall of azuki bean epicotyls. Plant Cell Physiol 42:154–161

    CAS  PubMed  Google Scholar 

  • Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35:585–657

    CAS  Google Scholar 

  • Takahashi Y, Nagata T (1992) Par B: an auxin-regulated gene encoding glutathione S-transferase. Proc Natl Acad Sci USA 89:56–59

    CAS  PubMed  Google Scholar 

  • Terry ME, Jones RI (1981) Effect of salt on auxin-induced acidification and growth by pea internode section. Plant Physiol 68:59–64

    CAS  Google Scholar 

  • Thiel G, Blatt MR, Fricker MD, White IR, Millner P (1993) Modulation of K+ channels in Vicia stomatal guard cells by peptide homologues to the auxin-binding proteins C-terminus. Proc Natl Acad Sci USA 90:11493–11497

    CAS  PubMed  Google Scholar 

  • Tode K, Lüthen H (2001) Fusicoccin- and IAA-induced elongation growth share the same pattern of K+ dependence. J Exp Bot 52:251–255

    Article  CAS  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849

    CAS  PubMed  Google Scholar 

  • Vara F, Serrano R (1982) Partial purification and properties of the proton-translocating ATPase in plant plasma membrane. J Biol Chem 257:12826–12830

    CAS  PubMed  Google Scholar 

  • Vesper MJ, Evans ML (1979) Nonhormonal induction of H+-efflux from plant tissues and its correlation with growth. Proc Natl Acad Sci USA 76:6366

    CAS  Google Scholar 

  • Vincken JP, York WS, Beldman G, Voragen AGJ (1997) Two general branching patterns of xyloglucan, XXXG and XXGG. Plant Physiol 114:9–13

    Article  CAS  PubMed  Google Scholar 

  • Waller F, Furuya M, Nick P (2002) OsARF1, an auxin response factor from rice, is auxin-regulated and classifies as a primary auxin responsive gene. Plant Mol Biol 50:415–425

    Article  CAS  PubMed  Google Scholar 

  • Went FW (1928) Wuchsstoff und Wachstum. Rec Trav Bot Neerl 25:1–116

    Google Scholar 

  • Xing T, Higgins VJ, Blumwald E (1996) Regulation of plant defense response to fungal pathogens: two types of protein kinase in the reversible phosphorylation of the host plasma membrane H+-ATPase. Plant Cell 8:555–564

    CAS  Google Scholar 

  • Yamamoto HY, Nakayama TOM, Chichester CO (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem 97:168–173

    CAS  Google Scholar 

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    Achim Hager

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Hager, A. Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116, 483–505 (2003). https://doi.org/10.1007/s10265-003-0110-x

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