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Molecular Biology Reports

, Volume 41, Issue 8, pp 5097–5108 | Cite as

Functional analyses of a putative plasma membrane Na+/H+ antiporter gene isolated from salt tolerant Helianthus tuberosus

  • Qing Li
  • Zhong Tang
  • Yibing Hu
  • Ling Yu
  • Zhaopu Liu
  • Guohua XuEmail author
Article

Abstract

Jerusalem artichokes (Helianthus tuberosus L.) can tolerate relatively higher salinity, drought and heat stress. In this paper, we report the cloning of a Salt Overly Sensitive 1 (SOS1) gene encoding a plasma membrane Na+/H+ antiporter from a highly salt-tolerant genotype of H. tuberosus, NY1, named HtSOS1 and characterization of its function in yeast and rice. The amino acid sequence of HtSOS1 showed 83.4 % identity with the previously isolated SOS1 gene from the Chrysanthemum crassum. The mRNA level in the leaves of H. tuberosus was significantly up-regulated by presence of high concentrations of NaCl. Localization analysis using rice protoplast expression showed that the protein encoded by HtSOS1 was located in the plasma membrane. HtSOS1 partially suppressed the salt sensitive phenotypes of a salt sensitive yeast strain. In comparison with wild type (Oryza sativa L., ssp. Japonica. cv. Nipponbare), the transgenic rice expressed with HtSOS1 could exclude more Na+ and accumulate more K+. Expression of HtSOS1 decreased Na+ content much larger in the shoot than in the roots, resulting in more water content in the transgenic rice than WT. These data suggested that HtSOS1 may be useful in transgenic approaches to improving the salinity tolerance of glycophyte.

Keywords

Helianthus tuberosus Oryza sativa Plasma membrane Na+/H+ antiporter Salt tolerance SOS1 

Notes

Acknowledgments

We thank Dr. Xiaohua Long for help in selecting and planting the salt-tolerant plant H. tuberosus, This study was financially supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions Project in Jiangsu Province of China.

Supplementary material

11033_2014_3375_MOESM1_ESM.doc (1.1 mb)
Supplementary material 1 (DOC 1,156 kb)

References

  1. 1.
    FAO (2008) FAO land and plant nutrition management service. http://www.fao.org/ag/agl/agll/spush/
  2. 2.
    Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51(1):463–499CrossRefGoogle Scholar
  3. 3.
    Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Shi HZ, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285(5431):1256–1258CrossRefPubMedGoogle Scholar
  6. 6.
    Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta 1446:149–155CrossRefPubMedGoogle Scholar
  7. 7.
    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 46:35–42CrossRefPubMedGoogle Scholar
  8. 8.
    Xia T, Apse MP, Aharon GS, Blumwald E (2002) Identification and characterization of a NaCl inducible vacuolar Na+/H+ antiporter in Beta vulgaris. Physiol Plant 116:206–212CrossRefPubMedGoogle Scholar
  9. 9.
    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(2):146–159CrossRefPubMedGoogle Scholar
  10. 10.
    Fukuda A, Chiba K, Maeda M, Nakamura A, Maeshima M, Tanaka Y (2004) Effect of salt and osmotic stresses on the expression of genes for the vacuolar H+-pyrophosphatase, H+-ATPase subunit A, and Na+/H+ antiporter from barley. J Exp Bot 55(397):585–594CrossRefPubMedGoogle Scholar
  11. 11.
    Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19(8):765–768CrossRefPubMedGoogle Scholar
  12. 12.
    Zhang HX, Hodson JN, Williams JP, Blumwald E (2001) Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci 98(22):12832–12836PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Wu CA, Yang GD, Meng QW, Zheng CC (2004) The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. Plant Cell Physiol 45(5):600–607CrossRefPubMedGoogle Scholar
  14. 14.
    Xue ZY, Zhi DY, Xue GP, Zhang H, Zhao YX, Xia GM (2004) Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Sci 167(4):849–859CrossRefGoogle Scholar
  15. 15.
    Yin XY, Yang AF, Zhang KW, Zhang JR (2004) Production and analysis of transgenic maize with improved salt tolerance by the introduction of AtNHX1 gene. Acta Bot Sin 46(7):854–861Google Scholar
  16. 16.
    Jha A, Joshi M, Yadav NS, Agarwal PK, Jha B (2011) Cloning and characterization of the Salicornia brachiata Na+/H+ antiporter gene SbNHX1 and its expression by abiotic stress. Mol Biol Rep 38(3):1965–1973CrossRefPubMedGoogle Scholar
  17. 17.
    Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151CrossRefPubMedGoogle Scholar
  18. 18.
    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(12):6896–6901PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    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(12):8436–8441PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Qiu QS, Barkla BJ, Vera-Estrella R, Zhu JK, Schumaker KS (2003) Na+/H+ exchange activity in the plasma membrane of Arabidopsis. Plant Physiol 132:1041–1052PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Wang X, Yang R, Wang B, Liu G, Yang C, Cheng Y (2011) Functional characterization of a plasma membrane Na+/H+ antiporter from alkali grass (Puccinellia tenuiflora). Mol Biol Rep 38(7):4813–4822CrossRefPubMedGoogle Scholar
  22. 22.
    Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8(4):617–627PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Qi Z, Spalding EP (2004) Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+/H+ antiporter during salinity stress. Plant Physiol 136(1):2548–2555PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Fraile-Escanciano A, Kamisugi Y, Cuming AC, Rodríguez-Navarro A, Benito B (2010) The SOS1 transporter of Physcomitrella patens mediates sodium efflux in planta. New Phytol 188(3):750–761CrossRefPubMedGoogle Scholar
  25. 25.
    Oh DH, Gong Q, Ulanov A, Zhang Q, Li Y, Ma W, Yun DJ, Bressan RA, Bohnert HJ (2007) Sodium Stress in the Halophyte Thellungiella halophila and Transcriptional Changes in a thsos1-RNA Interference Line. J Integr Plant Biol 49(10):1484–1496CrossRefGoogle Scholar
  26. 26.
    Wu YX, Ding N, Zhao X, Zhao MG, Chang ZQ, Liu JQ, Zhang LX (2007) Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica. Plant Mol Biol 65(1):1–11CrossRefPubMedGoogle Scholar
  27. 27.
    Xu HX, Jiang XY, Zhan KH, Cheng XY, Chen XJ, Pardo JM, Cui DQ (2008) Functional characterization of a wheat plasma membrane Na+/H+ antiporter in yeast. Arch Biochem Biophys 473(1):8–15CrossRefPubMedGoogle Scholar
  28. 28.
    Martínez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143(2):1001–1012PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Song AP, Lu JG, Jiang JF, Chen SM, Guan ZY, Fang WM, Chen FD (2012) Isolation and characterisation of Chrysanthemum crassum SOS1, encoding a putative plasma membrane Na+/H+ antiporter. Plant Biol 14(5):706–713CrossRefGoogle Scholar
  30. 30.
    An J, Song AP, Guan ZY, Jiang JF, Chen FF, Lou WH, Fang WM, Liu ZW, Chen SM (2014) The over-expression of Chrysanthemum crassum CcSOS1 improves the salinity tolerance of chrysanthemum. Mol Biol Rep  10.1007/s11033-014-3287-2
  31. 31.
    Olias R, Eljakaoui Z, Li J, De Morales Paza, Marin-Manzano MC, Pardo JM, Belver A (2009) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant, Cell Environ 32(7):904–916CrossRefGoogle Scholar
  32. 32.
    Newton PJ, Myers BA, West DW (1991) Reduction in growth and yield of Jerusalem artichoke caused by soil salinity. Irrig Sci 12:213–221CrossRefGoogle Scholar
  33. 33.
    Long XH, Mehta S, Liu ZP (2008) Effect of NO3–N enrichment on seawater stress tolerance of Jerusalem artichoke (Helianthus tuberosus). Pedosphere 18(1):113–123CrossRefGoogle Scholar
  34. 34.
    Tsuchiya T, Takesawa T, Kanzaki H, Nakamura I (2004) Genomic structure and differential expression of two tandem-arranged GSTZ genes in rice. Gene 335:141–149CrossRefPubMedGoogle Scholar
  35. 35.
    Jain M, Tyagi AK, Khurana JP (2006) Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics 88:360–371CrossRefPubMedGoogle Scholar
  36. 36.
    Tzfira T, Tian GW, Lacroix B, Vyas S, Li J, Leitner-Dagan Y, Krichevsky A, Taylor T, Vainstein A, Citovsky V (2005) pSAT vectors: a modular series of plasmids for autofluorescent protein tagging and expression of multiple genes in plants. Plant Mol Biol 57(4):503–516CrossRefPubMedGoogle Scholar
  37. 37.
    Bart R, Chern M, Park CJ, Bartley L, Ronald PC (2006) A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods 2(1):13PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Miao Y, Jiang L (2007) Transient expression of fluorescent fusion proteins in protoplasts of suspension cultured cells. Nat Protoc 2(10):2348–2353CrossRefPubMedGoogle Scholar
  39. 39.
    Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136CrossRefPubMedGoogle Scholar
  40. 40.
    Tang Z, Fan XR, Li Q, Feng HM, Miller AJ, Shen QR, Xu GH (2012) Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root influx. Plant Physiol 160:2052–2063PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Quintero FJ, Blatt MR, Pardo JM (2000) Functional conservation between yeast and plant endosomal Na+/H+ antiporters. FEBS Lett 471:224–228CrossRefPubMedGoogle Scholar
  42. 42.
    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 USA 99(13):9061–9066PubMedCentralCrossRefPubMedGoogle Scholar
  43. 43.
    Venema K, Belver A, Marín-Manzano MC, Rodríguez-Rosales MP, Donaire JP (2003) A novel intracellular K+/H+ antiporter related to Na+/H+ antiporters is important for K+ ion homeostasis in plants. J Biol Chem 278(25):22453–22459CrossRefPubMedGoogle Scholar
  44. 44.
    Ai PH, Sun SB, Zhao JN, Fan XR, Xin WJ, Guo Q, Yu L, Shen QR, Wu P, Miller AJXuGH (2009) Two rice phosphate transporters, OsPht1; 2 and OsPht1; 6, have different functions and kinetic properties in uptake and translocation. Plant J 57(5):798–809CrossRefPubMedGoogle Scholar
  45. 45.
    Upadhyaya NM, Surin B, Ramm K, Gaudron J, Schünmann PHD, Taylor W, Waterhouse PM, Wang MB (2000) Agrobacterium-mediated transformation of Australian rice cultivars Jarrah and Amaroo using modified promoters and selectable markers. Funct Plant Biol 27(3):201–210CrossRefGoogle Scholar
  46. 46.
    Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Horie T, Schroeder JI (2004) Sodium transporters in plants: diverse genes and physiological functions. Plant Physiol 136:2457–2462PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Nakayama H, Horie T, Yonamine I, Shinmyo A, Yoshida K (2005) Improving salt tolerance in plant cells. Plant Biotechnol 22(5):477–487CrossRefGoogle Scholar
  49. 49.
    Garciadeblás B, Haro R, Benito B (2007) Cloning of two SOS1 transporters from the seagrass Cymodocea nodosa. SOS1 transporters from Cymodocea and Arabidopsis mediate potassium uptake in bacteria. Plant Mol Biol 63(4):479–490CrossRefPubMedGoogle Scholar
  50. 50.
    Shi H, Lee B, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21(1):81–85CrossRefPubMedGoogle Scholar
  51. 51.
    Oh DH, Leidi E, Zhang Q, Hwang SM, Li Y, Quintero FJ, Jiang X, D’Urzo MP, Lee SY, Zhao Y, Bahk JD, Bressan RA, Yun DJ, Pardo JM, Bohnert HJ (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222PubMedCentralCrossRefPubMedGoogle Scholar
  52. 52.
    Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B (2012) The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biol 12:188PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124(3):941–948PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Katiyar-Agarwal S, Zhu JH, Kim KM, Agarwal M, Fu XM, Huang A, Zhu JK (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:18816–18821PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Kant S, Kant P, Raveh E, Simon B (2006) Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. Halophila. Plant, Cell Environ 29:1220–1234CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Qing Li
    • 1
    • 2
  • Zhong Tang
    • 1
    • 2
  • Yibing Hu
    • 1
    • 2
  • Ling Yu
    • 1
    • 2
  • Zhaopu Liu
    • 2
  • Guohua Xu
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Crop Genetics and Germplasm EnhancementNanjing Agricultural UniversityNanjingChina
  2. 2.MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze RiverNanjing Agricultural UniversityNanjingChina

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