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Overexpression of AeNHX1, a root-specific vacuolar Na+/H+ antiporter from Agropyron elongatum, confers salt tolerance to Arabidopsis and Festuca plants

  • Biotic and Abiotic Stress
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Abstract

Agropyron elongatum, a species in grass family, has a strong tolerance to salt stress. To study the molecular mechanism of Agropyron elongatum in salt tolerance, we isolated a homolog of Na+/H+ antiporters from the root tissues of Agropyron plants. Sequence analysis revealed that this gene encodes a putative vacuolar Na+/H+ antiporter and was designated as AeNHX1. The AeNHX1–GFP fusion protein was clearly targeted to the vacuolar membrane in a transient transfection assay. Northern analysis indicated that AeNHX1 was expressed in a root-specific manner. Expression of AeNHX1 in yeast Na+/H+ antiporter mutants showed function complementation. Further, overexpression of AeNHX1 promoted salt tolerance of Arabidopsis plants, and improved osmotic adjustment and photosynthesis which might be responsible for normal development of transgenic plants under salt stress. Similarly, AeNHX1 also functioned in transgenic Festuca plants. The results suggest that this gene might function in the roots of Agropyron plants, and its expression is involved in the improvement of salt tolerance.

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Abbreviations

GFP:

Green fluorescent protein

YPG:

Yeast extract/peptone/galactose

Pn:

Net photosynthetic rate

RWC:

Relative water content

References

  • Apes MP, Aharon GS, Snedden WA, Blumwald E (1998) In: Proceedings of the 11th international workshop on plant membrane biology, Cambridge, UK

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

    Article  Google Scholar 

  • Bettany AJE, Dalton SJ, Timms E, Manderyck B, Dhanoa MS, Morris P (2003) Agrobacterium tumefaciens-mediated transformation of Festuca arundinacea (Schreb.) and Lolium multiflorum (Lam.). Plant Cell Rep 21:437–444

    PubMed  CAS  Google Scholar 

  • Blumwald E, Poole RJ (1985) Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiol 78:163–167

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Brini F, Gaxiola RA, Berkowitz GA, Masmoudi K (2005) Cloning and characterization of a wheat vacuolar cation/proton antiporter and pyrophosphatase proton pump. Plant Physiol Biochem 43:347–354

    PubMed  CAS  Google Scholar 

  • Clarke MC, Wei W, Lindsey K (1992) High-frequency transformation of Arabidopsis thaliana by Agrobacterium tumefaciens. Plant Mol Biol Rep 10:178–189

    Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplied method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Elble R (1992) A simple and efficient procedure for transformation of yeast. Biotechniques 13:18–20

    PubMed  CAS  Google Scholar 

  • Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta 1446:149–155

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Glenn E, Brown JJ, Blumwald E (1999) Salt-tolerant mechanisms and crop potential of halophytes. Crit Rev Plant Sci 18:227–255

    Article  Google Scholar 

  • He C, Yan J, Shen G, Fu L, Scott Holaday A, Auld D, Blumwald E, Zhang H (2005) Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant Cell Physiol 46:1848–1854

    Article  PubMed  CAS  Google Scholar 

  • Hossain GS, Waditee R, Hibino T, Tanaka Y, Takabe T (2006) Root specific expression of Na+/H+ antiporter gene from Synechocystis sp. PCC6803 confers salt tolerance of tobacco plant. Plant Biotech 23: 275–281

    CAS  Google Scholar 

  • Lü SY, Jing YX, Shen SH, Zhao HY, Ma LQ, Zhou XJ, Ren Q, Li YF (2005) Antiporter gene from Hordeum brevisubulatum (Trin.) link and its overexpression in transgenic tobaccos. J Integr Plant Biol 47:343–349

    Article  Google Scholar 

  • Nass R, Rao R (1999) The yeast endosomal Na+/H+ exchanger, NHX1, confers osmotolerance following acute hypertonic shock. Microbiology 145:3221–3228

    PubMed  CAS  Google Scholar 

  • Orlowski J, Grinstein S (1997) Na+/H+ exchanger of mammalian cells. J Biol Chem 272:22373–22376

    Article  PubMed  CAS  Google Scholar 

  • Quintero FJ, Blatt MR, Pardo JM (2000) Functional conservation between yeast and plants endosomal Na+/H+ antiporters. FEBS Letters 471:224–228

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis TM (1989) Molecular cloning: a laboratory manual, 2nd edn. CSH Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Shi HZ, Ishitani M, Kim C, 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

    Article  PubMed  CAS  Google Scholar 

  • Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu J-K, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709

    Article  PubMed  CAS  Google Scholar 

  • Verslues PE, Bray EA (2004) LWR1 and LWR2 are required for osmoregulation and osmotic adjustment in Arabidopsis. Plant Physiol 136:2831–2842

    Article  PubMed  CAS  Google Scholar 

  • Wang BS, Lüttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J Exp Bot 52:2355–2365

    Article  PubMed  CAS  Google Scholar 

  • Wang ZN, Zhang JS, Guo BH, He SJ, Tian AG, Chen SY (2002) Cloning and characterization of the Na+/H+ antiport genes from Triticum aestivum. Acta Bot Sin 44:1203–1208

    CAS  Google Scholar 

  • Wang J, Zuo K, Wu W, Song J, Sun X, Lin J, Li X, Tang K (2004) Expression of a novel antiporter gene from Brassica napus resulted in enhanced salt tolerance in transgenic tobacco plants. Biol Plant 48:509–515

    Article  CAS  Google Scholar 

  • 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 45:600–607

    Article  PubMed  CAS  Google Scholar 

  • Wyn Jones RG, Pollard A (1983) Proteins, enzymes and inorganic ions. Encyclopedia of plant physiology. In: Lauchli A, Person A (eds) Springer, New York, pp 528–562

  • Xia GM, Xiang FN, Zhou AF, Wang HA, Chen HM (2003) Asymmetric somatic hybridization between wheat (Triticum aestivum L.) and Agropyron elongatum (Host). Theor Appl Genet 107:299–305

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Zhu J-K (2002) Salt tolerance. In: Somerville C, Meyerowitz E (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville

    Google Scholar 

  • Xue ZY, Zhi DY, Xue GP, Zhang H, Zhao YH, 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 167:849–859

    Article  CAS  Google Scholar 

  • 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 46:854–861

    CAS  Google Scholar 

  • Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30:529–539

    Article  PubMed  CAS  Google Scholar 

  • Zhang H-X, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768

    Article  PubMed  CAS  Google Scholar 

  • Zhang H-X, 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 USA 98:12832–12836

    Article  PubMed  CAS  Google Scholar 

  • Zhao XY, Liu MS, Li JR, Guan CM, Zhang XS (2005) The wheat TaGI1, involved in photoperoidic flowering, encodes an Arabidopsis GI ortholog. Plant Mol Biol 58:53–64

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Pardo (Consejo Superior de Investigacions Científicas, Spain) who kindly provided the yeast strain AXT3 to us. This research was supported by Project of Plant Transformation (JY03-A-02), and Program of “863” (2004AA212131) in China.

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Authors and Affiliations

  1. College of Life Sciences, Peking University, Beijng, 100871, China

    Wei Hua Qiao

  2. Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, Shandong, 271018, China

    Xiang Yu Zhao, Wei Li, Yan Luo & Xian Sheng Zhang

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  1. Wei Hua Qiao
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  2. Xiang Yu Zhao
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  3. Wei Li
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  4. Yan Luo
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  5. Xian Sheng Zhang
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Correspondence to Xian Sheng Zhang.

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Communicated by W.-H. Wu.

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Qiao, W.H., Zhao, X.Y., Li, W. et al. Overexpression of AeNHX1, a root-specific vacuolar Na+/H+ antiporter from Agropyron elongatum, confers salt tolerance to Arabidopsis and Festuca plants. Plant Cell Rep 26, 1663–1672 (2007). https://doi.org/10.1007/s00299-007-0354-3

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  • DOI: https://doi.org/10.1007/s00299-007-0354-3

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