Skip to main content
SpringerLink
Log in

Plant cells express several stress calcium ATPases but apparently no sodium ATPase

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The existence of plant Na+-ATPases has been investigated in barley (Hordeum vulgare) and in the seagrass Cymodocea nodosa, by a combination of RT–PCR and flux approaches. Systematic RT–PCR amplifications were carried out in mRNA preparations of barley roots exposed to Na+ or of Cymodocea leaves, using degenerate primers that can amplify all known plant and fungal Na+- and Ca2+-ATPases and animal Na+,K+-ATPases. This allowed the amplification of fourteen different cDNAs that could encode P-type ATPases. A phylogenetic analysis showed that none of these ATPases belongs to the ENA type, in which all fungal Na+-ATPases cluster, or to the animal Na+,K+-ATPase type, and that all cluster with known plant and fungal Ca2+-ATPases. Expression analysis of the barley transcripts indicates that the expressions of all but one of the ATPases are enhanced at high Ca2+, high pH, or high Na+, and that three ATPases are only expressed under stress conditions. Genes encoding ENA- or Na+,K+-ATPases were not found in the complete genomes of Arabidopsis thaliana and rice (Oryza sativa). On the basis of these results, we discuss the probable absence of Na+-ATPases in plants, and the function of Ca2+-ATPases that are expressed only under conditions of stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Almagro A, Prista C, Benito B, Lourero-Dias M C and Ramos J 2001 Cloning and expression of two genes coding for sodium pumps in the salt-tolerant yeast Debaryomyces hansenii. J. Bacteriol. 183, 3251–3255.

    Google Scholar 

  • Altschul S F, Gish W, Miller W, Myers E W and Lipman D J 1990 Basic local alignment search tool. J. Mol. Biol. 215, 403–410.

    Google Scholar 

  • Amtmann A and Sanders D 1999 Mechanisms of Na+ uptake by plant cells. Adv. Bot. Res. 29, 75–112.

    Google Scholar 

  • Antebi A and Fink G R 1992 The yeast Ca2+-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol. Biol. Cell 3, 633–654.

    Google Scholar 

  • Apse M P, Aharon G S, Snedden W A and Blumwald E 1999 Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256–1258.

    Google Scholar 

  • Axelsen K B and Palmgren M G 1998 Evolution of substrate specificities in the P-type ATPase superfamily. J. Mol. Evol. 46, 84–101.

    Google Scholar 

  • Bañuelos M A, Klein R D, Alexander-Bowman S J and Rodríguez-Navarro A 1995a A potassium transporter of the yeast Schwanniomyces occidentalis homologous to the Kup system of Escherichia coli has a high concentrative capacity. EMBO J. 14, 3021–3027.

    Google Scholar 

  • Bañuelos M A, Quintero F J and Rodríguez-Navarro A 1995b Functional expression of the ENA1 (PMR2)-ATPase of Saccharomyces cerevisiae in Schizosaccharomyces pombe. Biochim. Biophys. Acta 1229, 233–238.

    Google Scholar 

  • Bañuelos M A and Rodríguez-Navarro A 1998 P-type ATPases mediate sodium and potassium effluxes in Schwanniomyces occidentalis. J. Biol. Chem. 273, 1640–1646.

    Google Scholar 

  • Benito B, Garciadeblas B and Rodríguez-Navarro A 2000 Molecular cloning of the calcium and sodium ATPases in Neurospora crassa. Mol. Microbiol. 35, 1079–1088.

    Google Scholar 

  • Berridge M J, Bootman M D and Lipp P 1998 Calcium - a life and death signal. Nature 395, 645–648.

    Google Scholar 

  • Blumwald E, Aharon G S and Apse M P 2000 Sodium transport in plant cells. Biochim. Biophys. Acta 1465, 140–151.

    Google Scholar 

  • Clarke D M, Loo T W, Inesi G and MacLennan D H 1989 Location of high affinity Ca2+ - binding sites within the predicted transmembrane domain of the sarcoplasmic reticulum Ca2+-ATPase. Nature 339, 476–478.

    Google Scholar 

  • Cone K C, Burr F A and Burr B 1986 Molecular analysis of the maize anthocyanin regulatory locus. Proc. Natl. Acad. Sci. USA 83, 9631–9635.

    Google Scholar 

  • Cunningham K W and Fink G R 1994 Ca2+ transport in Saccharomyces cerevisiae. J. Exp. Biol. 196, 157–166.

    Google Scholar 

  • Darley C P, Wuytswinkel O C M v, Woude K v d and Mager W H 2000 Arabidopsis thaliana and Saccharomyces cerevisiae NHX1 genes encode amiloride sensitive electroneutral Na+/H+ exchangers. Biochim. J. 351, 241–249.

    Google Scholar 

  • Dürr G, Strayle J, Plemper R, Elbs S, Klee S K, Catty P, Wolf D H and Rudolph H K 1998 The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum associated protein degradation. Mol. Biol. Cell 9, 1149–1162.

    Google Scholar 

  • Evans D E and Williams L E 1998 P-type calcium ATPases in higher plants - biochemical, molecular and functional properties. Biochim. Biophys. Acta 1376, 1–25.

    Google Scholar 

  • Garciadeblas B, Rubio F, Quintero F J, Bañuelos M A and Rodríguez-Navarro A 1993 Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae. Mol. Gen. Genet. 236, 363–368.

    Google Scholar 

  • Geisler M, Axelsen K B, Harper J F and Palmgren M G 2000a Molecular aspects of higher plant Ca2+-ATPases. Biochim. Biophys. Acta 1465, 52–78.

    Google Scholar 

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

    Google Scholar 

  • Gunteski-Hamblin A, Clarke D M and Shull G E 1992 Molecular cloning and tissue distribution of alternatively spliced messenger RNAs encoding possible mammalian homologues of the yeast secretory pathway calcium pump. Biochemistry 31, 7600–7608.

    Google Scholar 

  • Haro R, Garciadeblas B and Rodríguez-Navarro A 1991 A novel P-type ATPase from yeast involved in sodium transport. FEBS Lett. 291, 189–191.

    Google Scholar 

  • Hassidim M, Braun Y, Lerner H R and Reinhold L 1990 Na+/H+ and K+/H+ antiport in root membrane vesicles isolated from the halophyte Atriplex and the glycophyte cotton. Plant Physiol. 94, 1795–1801.

    Google Scholar 

  • Hirschi K 2001 Vacuolar H+/Ca2+ transport: who's directing the traffic? Trends Plant Sci. 6, 100–104.

    Google Scholar 

  • Jacobsen T and Adams R M 1958 Salt and silt in ancient mesopotamian agriculture. Science 128, 1251–1258.

    Google Scholar 

  • Jaillard B, Guyon A and Maurin A 1991 Structure and composition of calcified roots, and their identification in calcareous soils. Geoderma 50, 197–210.

    Google Scholar 

  • Jeschke WD 1982 Shoot-dependent regulation and potassium fluxes in roots of whole barley seedlings. J. Exp. Bot. 33, 601–618.

    Google Scholar 

  • Jeschke W D and Stelter W 1973 K+-dependent net Na+ efflux in roots of barley plants. Planta 114, 251–258.

    Google Scholar 

  • Kang H A, Kim J-Y, Ko S-M, Park C S, Ryu D D Y, Sohn J-H, Choi E-S and Rhee S-K 1998 Cloning and characterization of the Hansenula polymorpha homologue of the Saccharomyces cerevisiae PMR1 gene. Yeast 14, 1233–1240.

    Google Scholar 

  • Katsuhara M, Yazaki Y, Sakano K and Kawasaki T 1997 Intracellular pH and proton-transport in barley root cells under salt stress: in vivo 31P-NMR study. Plant Cell Physiol. 38, 155–160.

    Google Scholar 

  • Kiegle E, Moore C A, Haseloff J, Tester M A and Knight M R 2000 Cell-type-specific calcium responses to drough, salt and cold in the Arabidopsis root. Plant J. 23, 267–278.

    Google Scholar 

  • Kiegle E A and Bisson M A 1996 Plasma membrane Na+ transport in a salt-tolerant Charophyte. Isotopic fluxes, electrophysiology, and thermodynamics in plant adapted to saltwater and freshwater. Plant Physiol. 111, 1191–1197.

    Google Scholar 

  • Knight H, Trewavas A J and Knight M R 1997 Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 12, 1067–1078.

    Google Scholar 

  • Lazof D B and Bernstein N 1999 The NaCl induced inhibition of shoot growth: the case for disturbed nutrition with special consideration of calcium. Adv. Bot. Res. 29, 113–189.

    Google Scholar 

  • Maathuis F J M and Amtmann A 1999 K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann. Bot. 84, 123–133.

    Google Scholar 

  • Marschner H. 1995. Mineral nutrition of higher plants. London: Academic Press. Mennen H, Jacoby B and Marschner H 1990 Is sodium proton antiport ubiquitous in plant cells.J. Plant. Physiol. 180–183.

    Google Scholar 

  • Møller J V, Juul B and Maire M l 1996 Structural organization, ion transport, and energy transduction of P-type ATPases. Biochim. Biophys. Acta 1286, 1–51.

    Google Scholar 

  • Niu X, Bressan R A, Hasegawa P M and Pardo J M 1995 Ion homeostasis in NaCl stress environments. Plant Physiol. 109, 735–742.

    Google Scholar 

  • Padam E and Schuldiner S 1994 Molecular biology of Na+/H+ antiporters: molecular devices that couple the Na+ and H+ circulation in cells. Biochim. Biophys. Acta 1187, 206–210.

    Google Scholar 

  • Park C S, Kim J-Y, Crispino C, Chang C C and Ryu D D Y 1998 Molecular cloning of YlPMR1, a S. cerevisiae PMR1 homologue encoding a novel P-type secretory pathway Ca2+-ATPase, in the yeast Yarrowia lipolytica. Gene 206, 107–116.

    Google Scholar 

  • Pérez-Prat E, Narasimhan M L, Binzel M L, Botella M A, Chen Z, Valpuesta V, Bressan R A and Hasegawa P M 1992 Induction of a putative Ca2+-ATPase mRNA in NaCl-adapted cells. Plant Physiol. 100, 1471–1478.

    Google Scholar 

  • Pittman J K, Mills R F, O'Connor C D and Williams L E 1999 Two additional type IIA Ca2+-ATPases are expressed in Arabidopsis thaliana: evidence that type IIA sub-groups exist. Gene 236, 137–147.

    Google Scholar 

  • Quintero F J, Blatt MR and Pardo JM 2000 Functional conservation between yeast and plant endosomal Na+/H+ antiporters. FEBS Lett. 471, 224–228.

    Google Scholar 

  • Rodríguez-Navarro A 2000 Potassium transport in fungi and plants. Biochim. Biophys. Acta 1469, 1–30.

    Google Scholar 

  • Rodríguez-Navarro A, Quintero F J and Garciadeblás B 1994 Na+-ATPases and Na+/H+ antiporters in fungi. Biochim. Biophys. Acta 1187, 203–205.

    Google Scholar 

  • Sanders D, Brownlee C and Harper J F 1999 Communicating with calcium. Plant Cell 11, 691–706.

    Google Scholar 

  • Serrano R 1988 Structure and function of proton translocating ATPase in plasma membranes of plants and fungi. Biochim. Biophys. Acta 947, 1–28.

    Google Scholar 

  • Shi H, Ishitani M, Kim C and Zhu J-K 2000 The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc. Natl. Acad. Sci. USA 97, 6896–6901.

    Google Scholar 

  • Shono M, Hara Y, Wada M and Fujii T 1996 A sodium pump in the plasma membrane of the marine alga Heterosigma akashiwo. Plant Cell Physiol. 37, 385–388.

    Google Scholar 

  • Shono M, Wada M and Fujii T. 1998. Characterization and molecular cloning of Na+-ATPase on plasma membrane of the marine raphidophycean Heterosigma akashiwo. In 11th International Workshop on Plant Membrane Biology. Cambridge, UK. Eds. Tester M, Morris C, Davies J, p 15. The Society for Experimental Biology.

  • Strayle J, Pozzan T and Rudolph H K 1999 Steady-state free Ca2+ in the yeast endoplasmic reticulum reaches only 10 µM and is mainly controlled by the secretory pathway pump Pmr1. EMBO J. 18, 4733–4743.

    Google Scholar 

  • Sudbrak R, Brown J, Dobson-Stone C, Ramser J, White J, Healy E, Dissanayake M, larrègue M, Perrussel M, Lehrach H, Munro C S, Strachan T, Burge S, Hovnanian A and Monaco A P 2000 Hailey Hailey disease is caused by mutations in ATP2C1 encoding a novel Ca2+ pump. Hum. Mol. Genet. 9, 1131–1140.

    Google Scholar 

  • Thompson J D 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882.

    Google Scholar 

  • Trewavas A 1999 Le calcium, c'est la vie: calcium makes waves. Plant Physiol. 120, 1–6.

    Google Scholar 

  • Tyerman S D and Skerrett I M 1999 Root ion channels and salinity. Sci. Hort. 78, 175–235.

    Google Scholar 

  • Walker D J, Black C R and Miller A J 1998 The role of cytosolic potassium and pH in the growth of barley roots. Plant Physiol. 118, 957–964.

    Google Scholar 

  • Watanabe Y, Iwaki T, Shimomno Y, Ichimiya A, Nagaoka Y and Tamai Y 1999 Characterization of the Na+-ATPase gene (ZENA1) from the salt-tolerant yeast Zygosaccharomyces rouxii. J. Biosci. Bioeng. 88, 136–142.

    Google Scholar 

  • Webb M A 1999 Cell-mediated crystallization of calcium oxalate in plants. Plant Cell 11, 751–761.

    Google Scholar 

  • White P J 1999 The molecular mechanism of sodium influx to root cells. Trends Plant Sci. 4, 245–246.

    Google Scholar 

  • Wilson C and Shannon M C 1995 Salt-induced Na+/H+ antiport in root plasma membrane of a glycophytic and halophytic species of tomato. Plant Sci. 107, 147–157.

    Google Scholar 

  • Wimmers L E, Ewing N E and Bennet A B 1992 Higher plant Ca2+-ATPase: primary structure and regulation of mRNA abundance by salt. Proc. Natl. Acad. Sci. USA 89, 9205–9209.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Biotecnología, Escuela Técnica Superior de Ingenieros Agrónomos, Universidad Politécnica de Madrid, 28040, Madrid, Spain

    B. Garciadeblas, B. Benito & A. Rodríguez-Navarro

Authors
  1. B. Garciadeblas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Benito
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Rodríguez-Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Rodríguez-Navarro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garciadeblas, B., Benito, B. & Rodríguez-Navarro, A. Plant cells express several stress calcium ATPases but apparently no sodium ATPase. Plant and Soil 235, 181–192 (2001). https://doi.org/10.1023/A:1011949626191

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011949626191

Search

Navigation