Abstract
The plasma membrane (PM) vesicles from Populus euphratica (P. euphratica) callus were isolated to investigate the properties of the PM H+-ATPase. An enrichment of sealed and oriented right-side-out PM vesicles was demonstrated by measurement of the purity and orientation of membrane vesicles in the upper phase fraction. Analysis of pH optimum, temperature effects and kinetic properties showed that the properties of the PM H+-ATPase from woody plant P. euphratica callus were consistent with those from herbaceous species. Application of various thiol reagents to the reaction revealed that reduced thiol groups were essential to maintain the PM H+-ATPase activity. In addition, there was increased H+-ATPase activity in the PM vesicles when callus was exposed to NaCl. Western blotting analysis demonstrated an enhancement of H+-ATPase content in NaCl-treated P. euphratica callus compared with the control.
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Abbreviations
- P. euphratica :
-
Populus euphratica
- PM:
-
Plasma membrane
- Triton X-100:
-
T-octyphenoxypoly-ethoxy ethanol
References
Arango M, Gévaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump-ATPase: the significance of gene subfamilies. Planta 216:355–365
Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Haeper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618–628
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Braun Y, Hassidim M, Lerner H, Reinhold L (1986) Salinity during growth modulates the proton pump in the halophyte Atriplex nummularia. Plant Physiol 81:1050–1056
Buckhout TJ, Bell PF, Luster DG, Chaney RL (1989) Iron-stress induced redox activity in tomato (Lycopersicum esculentum Mill.) is localized on the plasma membrane. Plant Physiol 90:151–156
Chen YN, Wang Q, Ruan X, Li WH, Chen YP (2004) Physiological response of Populus euphratica to artificial water-recharge of the lower reaches of tarim river. Acta Bot Sin 46:1393–1401
Cosgrove DJ (1997) Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell 9:1031–1041
Dean RT, Fu S, Stocker R, Davies MJ (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 324:1–18
Dracup M (1991) Increasing salt tolerance of plants through cell culture requires greater understanding of tolerance mechanisms. Aust J Plant Physiol 18:1–15
Ghezzi P (2005) Oxidoreduction of protein thiols in redox regulation. Biochem Soc T 33:1378–1381
Gu RS, Fonseca S, Puskás LG Jr LH, Zvara Á, Dudits D, Pais MS (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiol 24:265–276
Hernández A, Cooke DT, Clarkson DT (1994) Lipid composition and proton transport in Penicillium cyclopium and Ustilago maydis plasma membrane vesicles isolated by two-phase partitioning. Biochim Biophys Acta 1195:103–109
Hodges TK, Leonard RT, Bracker CE, Keenan TW (1972) Purification of an ion-stimulated adenosine triphosphatase from plant roots: association with plasma membranes. Proc Natl Acad Sci USA 69:3307–3311
Kalampanayil BD, Wimmers LE (2001) Identification and characterization of a salt-stress-induced plasma membrane H+-ATPase in tomato. Plant Cell Environ 24:999–1005
Kasamo K (1986) Comparison of plasma membrane and tonoplast H+-translocating ATPase in Phaseolus mungo L. roots. Plant Cell Physiol 27:49–59
Kerkeb L, Donaire JP, Rodriguez-Rosales MP (2001a) Plasma membrane H+-ATPase activity is involved in adaption of tomato calli to NaCl. Physiol Plant 111:483–490
Kerkeb L, Donaire JP, Venema K, Rodriguez-Rosales MP (2001b) Tolerance to NaCl induces changes in plasma membrane lipid composition, fluidity and H+-ATPase of tomato calli. Physiol Plant 113:217–224
Kjellbom P, Larsson C (1984) Preparaction and polypeptide compolisition of chlorophyii-free plasma membranes from leaves of light-grown spinach and barley. Physiol Plant 62:501–509
Kuhlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5:282–295
Krysan PJ, Young JC, Tax F, Sussman MR (1996) Identification of transferred DNA insertions within Arabidopsis genome is involved in signal transduction and ion transport. Proc Natl Acad Sci USA 93:8145–8150
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Larsson C, Widel lS, Kjellbom P (1987) Preparation of high-purity plasma membrane. Method Enzymol 148:558–568
Michelet B, Boutry M (1995) The plasma membrane H+-ATPase: a highly regulated enzyme with multiple physiological functions. Plant Physiol 108:1–6
Morsomme P, Boutry M (2000) The plant plasma membrane H+-ATPase: structure, function and regulation. Biochim Biophys Acta 1465:1–16
Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl environments. Plant Physiol 190:735–742
Niu X, Narasimhan ML, Salzman RA, Bressan RA, Hasegawa PM (1993a) NaCl regulation of plasma membrane H+-ATPase gene expression in a glycophyte and a halophyte. Plant Physiol 103:713–718
Niu X, Zhu JK, Narasimham ML, Bressan RA, Hasegawa PM (1993b) Plasma membrane H+-ATPase gene expression is regulated by NaCl in halophyte (Atriplex nummularia L.) cell cultures. Planta 190:433–438
Ohnishi T, Gall RS, Mayer ML (1975) An improved assay of inorganic phosphate in the presence of extralabile phosphate compounds: application to the ATPase assay in the presence of phosphocratine. Anal Biochem 69:261–267
Olivari C, Meanti C, De Michelis MI, Rasi-Caldogno F (1998) Fusicoccin binding to its plasma membrane receptor and the activation of the plasma membrane H+-ATPase. Plant Physiol 116:529–537
Örtegren U, Karlsson M, Blazic N, Blomqvist M, Nystrom FH, Gustavsson J, Fredman P, Strålfors P (2004) Lipids and glycosphingolipids in caveolae and surrounding plasma membrane of primary rat adipocytes. Eur J Biochem 271:2028–2036
Palmgren MG (1998) Proton gradients and plant growth: role of the plasma membrane H+-ATPase. Adv Bot Res 28:1–70
Porillo F (2000) Regulation of plasma membrane H+-ATPase in fungi and plants. Biochim Biophys Acta 1469:31–42
Reinhold L, Seiden A, Volokita M (1984) Is modulation of the rate of proton pumping a key event in osmoregulation? Plant Physiol 75: 846–849
Rober-Kleber N, Albrechtov JTP, Fleig S, Huck N, Michalke W, Wagner E, Speth V, Neuhaus G, Fischer-Iglesias C (2003) Plasma membrane H+-ATPase is involved in auxin-mediated cell elongation during wheat embryo development. Plant Physiol 131:1302–1312
Serrano R (1989) Structure and function of plasma membrane ATPase. Annu Rev Plant Physiol 40:61–94
Shimogawara K, Usuda H (1993) A concebtrating two-phase partitioning: its application to isolation of plasma membrane from maize roots. Anal Biochem 212:381–387
Sibole JV, Cabot C, Michalke W, Poschenrieder C, Barceló J (2005) Relationship between expression of the PM H+-ATPase, growth and ion partitioning in the leaves of salt-treated Medicago species. Planta 221:557–566
Sondegaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482
Tavakoli N, Kluge C, Golblack D, Mimuura T, Dietz KJ (2001) Reversible redox control of plant vacuolar H+-ATPase activity is related to disulfide bridge formation in subunit E as well as subunit A. Plant J 28:51–59
Wu J, Seliskar D (1998) Salinity adaptation of plasma membrane H+-ATPase in the salt marsh plant Spartina patens: ATP hydrolysis and enzyme kinetics. J Exp Bot 49:1005–1013
Yoshida S, Kawata T, Uemura M, Niki T (1986) Properties of plasma membrane isolated from chilling-sensitive etiolated seedlings of Vigna radiata L.. Plant Physiol 80:152–160
Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857
Zhao R, Dielen F, Kinet JM, 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
Zhang F, Yang YL, He WL, Zhao X, Zhang LX (2004) Effects of salinity on growth and compatible solutes of callus induced from Populus euphratica. In Vitro Cell Dev Biol Plant 40:491–494
Acknowledgements
We are grateful to Dr. R. Serrano for his generosity to provide the antibody against H+-ATPase. This work is financially supported by the Gansu project for science and technology (2GS035-A41-001-06); 2006 Gansu Natural Science project the National Natural Science Foundtion of China, major science project for eco-environment in the western regions of china (90302010); Ministry of Communications of China, Science and Technology Project for Traffic Construction in West China; Chinese postdoctoral science project (2005037164).
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Communicated by R. J. Rose
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Yang, Y., Zhang, F., Zhao, M. et al. Properties of plasma membrane H+-ATPase in salt-treated Populus euphratica callus. Plant Cell Rep 26, 229–235 (2007). https://doi.org/10.1007/s00299-006-0220-8
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DOI: https://doi.org/10.1007/s00299-006-0220-8