Skip to main content
SpringerLink
Log in

Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Populus euphratica is a salt-tolerant tree species growing in semi-arid saline areas. A Na+/H+ antiporter gene was successfully isolated from this species through RACE cloning, and named PeSOS1. The isolated cDNA was 3665 bp long and contained a 3438 bp open reading frame that was predicted to encode a 127-kDa protein with 12 hypothetical transmembrane domains in the N-terminal part and a long hydrophilic cytoplasmic tail in the C-terminal part. The amino acid sequence of this PeSOS1 gene showed 64% identity with the previously isolated SOS1 gene from the glycophyte Arabidopsis thaliana. The level of protein expressed by PeSOS1 in the leaves of P. euphratica was significantly up-regulated in the presence of high (200 mM) concentrations of NaCl, while the mRNA level in the leaves remained relatively constant. Immunoanalysis suggested that the protein encoded by PeSOS1 is localized in the plasma membrane. Expression of PeSOS1 partially suppressed the salt sensitive phenotypes of the EP432 bacterial strain, which lacks the activity of the two Na+/H+ antiporters EcNhaA and EcNhaB. These results suggest that PeSOS1 may play an essential role in the salt tolerance of P. euphratica and may be useful for improving salt tolerance in other tree species.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Apse MP, Aharon GS, Sneddon WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Article  PubMed  CAS  Google Scholar 

  • Banuelos MA, Ruiz MC, Jimenez A, Souciet JL, Potier S, Ramos J (2002) Role of the Nha1 antiporter in regulating K+ influx in Saccharomyces cerevisiae. Yeast 19:9–15

    Article  PubMed  CAS  Google Scholar 

  • Benito B, Garciadeblas B, Rodriguez-Navarro A (2002) Potassium-or sodium- efflux ATPase, a key enzyme in the evolution of fungi. Microbiology 148:933–941

    PubMed  CAS  Google Scholar 

  • Benito B, Rodriguez-Navarro A (2003) Molecular cloning and characterization of a sodium-pump ATPase of the moss Physcomitrella patens. Plant J 36:382–389

    Article  PubMed  CAS  Google Scholar 

  • Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151

    Article  PubMed  CAS  Google Scholar 

  • Bohnert HJ, Cushman JC (2000) The ice plant cometh: Lessons in abiotic stress tolerance. J Plant Growth Regul 19:334–346

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Ann Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Brett CL, Wei Y, Donowitz M, Rao R (2002) Human Na+/H+ exchanger isoform 6 is found in recycling endosomes of cells, not in mitochondria. Amer J Physiol Cell Physiol 282:C1031–C1041

    CAS  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Chen S, Li J, Wang S, Fritz E, Huttermann A, Altman A (2003) Effects of NaCl on shoot growth, transpiration, ion compartmentation, and transport in regenerated plants of Populus euphratica and Populus tomentosa. Can J For Res 33:967–975

    Article  CAS  Google Scholar 

  • Dibrov P, Smith JJ, Young PG, Larry F (1997) Identification and localization of the SOD2 gene product in fission yeast. FEBS Lett 405:119–124

    Article  PubMed  CAS  Google Scholar 

  • Dower WJ, Miller JF, Ragscale CW (1988) High efficiency transformation of E. coli by high voltage transformation. Nucl Acids Res 16:6127–6145

    Article  PubMed  CAS  Google Scholar 

  • Dzioba J, Ostroumov E, Winogrodzki A, Dibrov P (2002) Cloning, functional expression in Escherichia coli and primary characterization of a new Na+/H+ antiporter, NhaD, of Vibrio cholerae. Mol Cell Biochem 229:119–124

    Article  PubMed  CAS  Google Scholar 

  • Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45:146–159

    Article  PubMed  CAS  Google Scholar 

  • Gao XZ, Zhao RY, Zhang H (2003) Overexpression of SOD2 increases salt tolerance of Arabidopsis. Plant Physiol 133:1873–1881

    Article  PubMed  CAS  Google Scholar 

  • Garciadeblas B, Senn ME, Banuelos MA, Rodriguez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34:788–801

    Article  PubMed  CAS  Google Scholar 

  • Gaxiola RA, Rao R, Sherman GP, Alper SL, Fink GR (1999) The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci 96:1480–1485

    Article  PubMed  CAS  Google Scholar 

  • Gu R, Liu Q, Pei D, Jiang X (2004a) Understanding saline and osmotic tolerance of Populus euphratica suspended cells. Plant Cell Tiss Org Cult 78:261–265

    Article  CAS  Google Scholar 

  • Gu R, Fonseca S, Puskas LG, Hackler LJ, Zvara A, Dudits D, Pais MS (2004b) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiol 24:265–276

    PubMed  CAS  Google Scholar 

  • Hamada A, Shono M, Xia T, Ohta M, Hayashi Y, Tanaka A, Hayakawa T (2001) Isolation and characterization of a Na+/H+ antiporter gene from the halophyte Atriplex gmelini. Plant Mol. Biol 46:35–42

    Article  PubMed  CAS  Google Scholar 

  • Haro R, Banuelos MA, Senn ME, Barrero-Gil J, Rodryguez-Navarro A (2005) HKT1 mediates sodium uniport in roots. Pitfalls in the expression of HKT1 in Yeast. Plant Physiol 139:1495–1506

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Ann Rev Plant Physiol 51:463–499

    Article  CAS  Google Scholar 

  • Horie T, Schroeder JI (2004) Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol 136:2457–2462

    Article  PubMed  CAS  Google Scholar 

  • Hukin D, Cochard H, Dreyer E, Le-Thiec D, Bogeat-Triboulot MB (2005) Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? J Exp Bot 56:2003–2010

    Article  PubMed  CAS  Google Scholar 

  • Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, Shi H, Damsz B, Charbaji T, Gong Q, Ma S, Fredricksen M, Galbraith DW, Jenks MA, Rhodes D, Hasegawa PM, Bohnert HJ, Joly RJ, Bressan RA, Zhu JK (2004) Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135:1718–1737

    Article  PubMed  CAS  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  PubMed  CAS  Google Scholar 

  • Ivey DM, Gufanti AA, Zemsky J, Pinner E, Karpel R, Padan E, Schuldiner S, Krulwich TA (1993) Cloning and characterization of a putative Ca2+/H+ antiporter gene from Escherichia coli upon functional complementation of Na+/H+ antiporter- deficient strain by the over expressed gene. J Biol Chem 268:11296–11303

    PubMed  CAS  Google Scholar 

  • Karpel R, Olami Y, Taglicht D, Schuldiner S, Padan E (1988) Sequencing of the gene ant which affects the Na+/H+ antiporter activity in Escherichia coli. J Biol Chem 263:10408–10414

    PubMed  CAS  Google Scholar 

  • Ma H, Fung L, Wang S, Altman A, Huttermann A (1997) Photosynthetic response of Populus euphratica to salt stress. For Ecol Manag 93:55–61

    Article  Google Scholar 

  • Ma TJ, Liu QL, Li Z, Zhang XJ (2002) Tonoplast H+-ATPase in response to salt stress in Populus euphrastica cell suspensions. Plant Sci 163:499–505

    Article  CAS  Google Scholar 

  • Nakayama H, Horie T, Yonamine I, Shinmyo A, Yoshida K (2005) Improving salt tolerance in plant cells. Plant Biotech 22:477–487

    CAS  Google Scholar 

  • Nakamura N, Tanaka S, Teko Y, Mitsui K, Kanazawa H (2005) Four Na+/H+ exchanger isoforms are distributed to Golgi and post-Golgi compartments and are involved in organelle pH regulation. J Biol Chem 280:1561–1572

    Article  PubMed  CAS  Google Scholar 

  • Nass R, Cunningham KW, Rao R (1997) Intracellular sequestration of sodium by a novel Na+/H+ exchanger in yeast is enhanced by mutations in the plasma membrane H+-ATPase. J Biol Chem 272:26145–26152

    Article  PubMed  CAS  Google Scholar 

  • Nass R, Rao R (1998) Novel localization of a Na+/H+ exchanger in a late endosomal compartment of yeast. J Biol Chem 273:21054–21060

    Article  PubMed  CAS  Google Scholar 

  • Niu XM, Damsz B, Kononowicz AK, Bressan RA, Hasegawa PM (1996) NaCl-lnduced alterations in both cell structure and tissue- specific plasma membrane H+-ATPase gene expression. Plant Physiol 111:679–686

    PubMed  CAS  Google Scholar 

  • Nozaki K, Kuroda T, Mizushima T, Tsuchiya T (1998) A new Na+/H+ antiporter, NhaD, of Vibrio parahaemolyticus. Biochim Biophys Acta 1369:213–220

    Article  PubMed  CAS  Google Scholar 

  • Ohta M Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett 532:279–282

    Article  Google Scholar 

  • Ottow EA, Polle A, Brosche M, Kangasja J, Dibrov PC, Teichmann T (2005) Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin. Plant Mol Biol 58:75–88

    Article  PubMed  CAS  Google Scholar 

  • Padan E, Maisler N, Taglicht D, Karpel R, Schuldiner S (1989) Deletion of ant in Escherichia coli reveals its function in adaptation to high salinity and an alternative sodium proton antiporter system. J Biol Chem 264:20297–20302

    PubMed  CAS  Google Scholar 

  • Padan E, Schuldiner S (1994) Molecular physiology of the Na+/H+ antiporter in E. coli. J Exp Biol 196:443–456

    PubMed  CAS  Google Scholar 

  • Pinner E, Padan E, Schuldiner S (1992) Cloning sequencing and expression of the nhaB gene encoding a sodium proton antiporter in Escherichia coli. J Biol Chem 267:11064–11068

    PubMed  CAS  Google Scholar 

  • Prior C, Potier S, Souciet JL, Sychrova H (1996) Characterization of the NHA1 gene encoding a Na+/H+-antiporter of the yeast Saccharomyces cerevisiae. FEBS Lett 387:89–93

    Article  PubMed  CAS  Google Scholar 

  • Qiu QS, Su XF (1998) The influence of extracellular side Ca2+ on the activity of the plasma membrane H+-ATPase from wheat roots. Aust J Pl Physiol 25:923–928

    CAS  Google Scholar 

  • Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci. 99:8436–8441

    Article  PubMed  CAS  Google Scholar 

  • Qiu QS, Barkla BJ, Vera-Estrella R, Zhu JK, Schumaker KS (2003) Na+/H+ exchange activity in the plasma membrane of Arabidopsis. Plant Physiol 132:1041–1052

    Article  PubMed  CAS  Google Scholar 

  • Qiu QS, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, Zhu JK (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the Salt-Overly-Sensitive (SOS) pathway. J Biol Chem 279:207–215

    Article  PubMed  CAS  Google Scholar 

  • Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci 99:9061–9066

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Liu W (1999) Molecular pieces to the puzzle of the interaction between potassium and sodium uptake in plants. Trends Plant Sci 4:281–286

    Article  PubMed  Google Scholar 

  • Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci 97:6896–6901

    Article  PubMed  CAS  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477

    Article  PubMed  CAS  Google Scholar 

  • Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Mizoguchi T, Uraro T, Katagiri T, Nakashima K, Abe H, Ichimura K, Liu QA, Nanjyo T, Uno Y, Luchi S, Srki M, Lto T, Hirayama T, Mikami K (1998) Molecular responses to water stress in Arabidopsis thaliana. J Plant Res 111:345–351

    Article  CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  PubMed  CAS  Google Scholar 

  • Utsugi J, Inaba K, Kuroda T, Tsuda M, Tsuchiya T (1998) Cloning and sequencing of a novel Na+/H+ antiporter gene from Pseudomonas aeruginosa. Biochim Biophys Acta 1398:330–334

    PubMed  CAS  Google Scholar 

  • Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:1–10

    Article  CAS  Google Scholar 

  • Wang S, Chena B, Li H (1996) Euphrates poplar forest. Chinese Environmental Science Press, Beijing, pp 41–153

    Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  PubMed  CAS  Google Scholar 

  • Wu L, Fan Z, Guo L, Li Y, Chen ZL, Qu LJ (2005) Overexpression of the bacterial nhaA gene in rice enhances salt and drought tolerance. Plant Sci. 168:297–302

    Article  CAS  Google Scholar 

  • Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and Potassium acquisition. Plant Cell 8:617–627

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

    Article  CAS  Google Scholar 

  • Yang YL, Zhang F, He WL, Wang XM, Zhang LX (2003) Iron induced inhibition of H+-ATPase in plasma membrane vesicles isolated from wheat roots. Cell Mol Life Sci 60:1249–1257

    PubMed  CAS  Google Scholar 

  • Yang YL, Guo JK, Zhang F, Zhao LQ, Zhang LX (2004) NaCl induced changes of the H+-ATPase in root plasma membrane of two wheat cultivars. Plant Sci 166:913–918

    Article  CAS  Google Scholar 

  • Zhang HX, Blumwald E (2001) Tansgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit Nature Biotech 19:765–768

    Article  CAS  Google Scholar 

  • Zhang F, Yang YL, He WL, Zhao X, Zhang LX (2004) Effects of salinity on growth, compatible solutes of callus induced from Populus euphratica. In Vitro Cellul and Devel Biol 40:491–494

    CAS  Google Scholar 

  • Zhao MG, Zhao X, Wu YX, Zhang LX (2007) Enhanced sensitivity to oxidative stress in Arabidopsis nitric oxide synthase mutant. J Plant Physiol 164(6):737–745

    Google Scholar 

  • Zhu JK, Shi J, Singh U, Wyatt SE, Bressan RA, Hasegawa PM, Capita NC (1993) Enrichment of vitronectin and fibronectin like proteins in NaCl-adapted plant cells and evidence for their involvement in plasma membrane-cell wall adhesion. Plant J 3:637–646

    Article  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 4:401–406

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Etana Padan (the Hebrew University of Jerusalem) for providing the EP432 bacterial strain and Dr. Ramon Serrano for providing the antibody against PM H+-ATPase. Financial support for this research was provided by the National Science Foundation of China (Grant numbers: 30430560 and 40501012).

Author information

Authors and Affiliations

  1. Cold and Arid Regions Environment and Engineering Research Institute, The Chinese Academy of Sciences, Lanzhou, 730000, P.R. China

    Yuxia Wu, Xin Zhao & Zongqiang Chang

  2. Institute of Molecular Ecology, MOE Key Laboratory of Arid and Grassland Ecology, Lanzhou University, Lanzhou, 730000, P.R. China

    Yuxia Wu, Nan Ding & Jianquan Liu

  3. Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, P.R. China

    Mingui Zhao & Lixin Zhang

Authors
  1. Yuxia Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nan Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xin Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mingui Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zongqiang Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jianquan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lixin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lixin Zhang.

Additional information

Yuxia Wu and Nan Ding contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, Y., Ding, N., Zhao, X. et al. Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica . Plant Mol Biol 65, 1–11 (2007). https://doi.org/10.1007/s11103-007-9170-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-007-9170-y

Keywords

Search

Navigation