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Overexpression of Arabidopsis thaliana Na+/H+ antiporter gene enhanced salt resistance in transgenic poplar (Populus × euramericana ‘Neva’)

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Abstract

Salinity is a major abiotic stress factor limiting plant growth and productivity. One possible method to enhance plant salt-resistance is to compartmentalize sodium ions away from the cytosol. In the present work, a vacuolar Na+/H+ antiporter gene AtNHX1 from Arabidopsis thaliana, was transferred into Populus × euramericana ‘Neva’ by Agrobacterium tumefaciens in order to enhance poplar salt-resistance. The results showed that the transgenic poplar were more resistant to NaCl than the wild-type (WT) in greenhouse condition. Compared with the WT, plant growth and photosynthetic capacity of the transgenic plants were enhanced, and the transgenic plants accumulated more Na+ and K+ in roots and leaves under the same NaCl condition, whereas malondialdehyde and relative electrical conductivity were lower. All of these properties of the transgenic poplar were likely to be a consequence of the overexpression of AtNHX1 caused Na+ sequestration in the vacuoles and improved K+ absorption, thus reducing their toxic effects. These results indicated overexpression of the AtNHX1 enhanced salt-resistance of poplar, and AtNHX1 played an important role in the compartmentation of Na+ into the vacuoles. Therefore, this study provides an effective way for improving salt resistance in trees.

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Abbreviations

AtNHX1 :

Tonoplast-associated Na+/H+ antiporter gene of Arabidopsis

C a :

Atmospheric CO2 concentration

C i :

Intercellular CO2 concentration

DW:

Dry weight

F v/F m :

Maximum photochemical efficiency of PSII

G s :

Stomatal conductance

MDA:

Malondialdehyde

nptII :

Neomycin phosphotransferase II gene

P n :

Net photosynthetic rate

REC:

Relative electrical conductivity

RT-PCR:

Reverse transcription

TR:

Transgenic poplar

WT:

Wild-type poplar

References

  • Adams P, Thomas JC, Vernon DM, Bohnert HJ, Jensen RG (1992) Distinct cellular and organismic responses to salt stress. Plant Cell Physiol 33:1215–1223

    CAS  Google Scholar 

  • Apse MP, Aharon GS, Snedden 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 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Bayuelo-Jiménez JS, Debouck DG, Lynch JP (2003) Growth, gas exchange, water relations, and ion composition of Phaseolus species grown under saline conditions. Field Crop Res 80:207–222

    Article  Google Scholar 

  • Belkhodja R, Morales F, Abadía A, Gómez-Aparisi J, Abadía J (1994) Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.). Plant Physiol 104:667–673

    PubMed  CAS  Google Scholar 

  • Bradshaw HD Jr, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19:306–313

    Article  CAS  Google Scholar 

  • Chen LH, Zhang B, Xu ZQ (2008) Salt tolerance conferred by overexpression of Arabidopsis vacuolar Na+/H+ antiporter gene AtNHX1 in common buckwheat (Fagopyrum esculentum). Transgenic Res 17:121–132

    Article  PubMed  CAS  Google Scholar 

  • Glenn EP, Brown JJ (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255

    Article  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190

    Article  CAS  Google Scholar 

  • Hamzeh M, Dayanandan S (2004) Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast TRNT-TRNF region and nuclear rDNA. Am J Bot 91:1398–1408

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • He C, Yan J, Shen G, Fu L, Holaday AS, 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 

  • Hu L, Lu H, Liu QL, Chen XM, Jiang XN (2005) Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiol 25:1273–1281

    Article  PubMed  CAS  Google Scholar 

  • Imada S, Yamanaka N, Tamai S (2009) Effects of salinity on the growth, Na partitioning, and Na dynamics of a salt-tolerant tree, Populus alba L. J Arid Environ 73:245–251

    Article  Google Scholar 

  • Jiang XY, Leidi EO, Pardo JM (2010) How do vacuolar NHX exchangers function in plant salt tolerance? Plant Signal Behav 5:792–795

    Article  PubMed  CAS  Google Scholar 

  • Kramer D (1983) The possible role of transfer cells in the adaptation of plants to salinity. Physiol Plant 58:549–555

    Article  CAS  Google Scholar 

  • Leidi EO, Barragán V, Rubio L, El-Hamdaoui RuizMT, Cubero B, Fernández JA, Bressan RA, Hasegawa PM, Quintero FJ, Pardo JM (2010) The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J 61:495–506

    Article  PubMed  CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  • Lv S, Zhang K, Gao Q, Lian L, Song Y, Zhang J (2008) Overexpression of an H+-PPase gene from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant Cell Physiol 49:1150–1164

    Article  PubMed  CAS  Google Scholar 

  • Ma HC, Fung L, Wang SS, Altman A, Hüttermann A (1997) Photosynthetic response of Populus euphratica to salt stress. Forest Ecol Manag 93:55–61

    Article  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  PubMed  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Netondo GW, Onyango JC, Beck E (2004) Sorghum and salinity: II. Gas exchange and chlorophyll fluorescence of sorghum under salt stress. Crop Sci 44:806–811

    Article  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  PubMed  CAS  Google Scholar 

  • Peever TL, Higgins VJ (1989) Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from Cladosporium fulvum. Plant Physiol 90:867–875

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sibole JV, Montero E, Cabot C, Poschenrieder C, Barceló J (1998) Role of sodium in the ABA-mediated long-term growth response of bean to salt stress. Physiol Plant 104:299–305

    Article  CAS  Google Scholar 

  • Singh AK, Dubey RS (1995) Changes in chlorophyll a and b contents and activities of photosystems 1 and 2 in rice seedlings induced by NaCl. Photosynthetica 31:489–499

    CAS  Google Scholar 

  • Storey R (1995) Salt tolerance, ion relations and the effect of root medium on the response of citrus to salinity. Aust J Plant Physiol 22:101–114

    Article  CAS  Google Scholar 

  • Sultana N, Ikeda T, Itoh R (1999) Effect of NaCl salinity on photosynthesis and dry matter accumulation in developing rice grains. Environ Exp Bot 42:211–220

    Article  CAS  Google Scholar 

  • Taylor G (2002) Populus: Arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689

    Article  PubMed  CAS  Google Scholar 

  • van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  Google Scholar 

  • Venema K, Quintero FJ, Pardo JM, Donaire JP (2002) The Arabidopsis Na+/H+ exchanger AtNHX1 catalyzes low affinity Na+ and K+ transport in reconstituted liposomes. J Biol Chem 277:2413–2418

    Article  PubMed  CAS  Google Scholar 

  • Wang R, Chen S, Deng L, Fritz E, Huettermann A, Polle A (2007) Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars. Trees Struct Funct 21:581–591

    Article  CAS  Google Scholar 

  • Wang SY, Chen QJ, Wang WL, Wang XC, Lu MZ (2005) Salt tolerance conferred by over-expression of OsNHX1 gene in Poplar 84K. Chinese Sci Bull 50:224–228

    Article  CAS  Google Scholar 

  • Wang YC, Qu GZ, Li HY, Wu YJ, Wang C, Liu GF, Yang CP (2010) Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii. Mol Biol Rep 37:1119–1124

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  PubMed  CAS  Google Scholar 

  • Ye CY, Zhang HC, Chen JH, Xia XL, Yin WL (2009) Molecular characterization of putative vacuolar NHX-type Na+/H+ exchanger genes from the salt-resistant tree Populus euphratica. Physiol Plant 137:166–174

    Article  PubMed  CAS  Google Scholar 

  • Zhang HX, 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 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 USA 98:12832–12836

    Article  PubMed  CAS  Google Scholar 

  • Zhao GQ, Ma BL, Ren CZ (2007) Growth, gas exchange, chlorophyll fluorescence, and ion content of naked oat in response to salinity. Crop Sci 47:123–131

    Article  CAS  Google Scholar 

  • Zheng QS, Liu L, Liu ZP, Chen JM, Zhao GM (2009) Comparison of the response of ion distribution in the tissues and cells of the succulent plants Aloe vera and Salicornia europaea to saine stress. J Plant Nutr Soil Sci 172:875–883

    Article  CAS  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

Acknowledgments

We thank the National Key Project of Scientific and Technical Supporting Programs funded by the Ministry of Science and Technology of China (No. 2006BAD09A08-03-01) and the National High Technology Research and Development Program (863 Program) of China (No. 2007AA091702) supported the research.

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Correspondence to Zhaopu Liu.

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Communicated by U. Luettge.

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Jiang, C., Zheng, Q., Liu, Z. et al. Overexpression of Arabidopsis thaliana Na+/H+ antiporter gene enhanced salt resistance in transgenic poplar (Populus × euramericana ‘Neva’). Trees 26, 685–694 (2012). https://doi.org/10.1007/s00468-011-0635-x

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  • DOI: https://doi.org/10.1007/s00468-011-0635-x

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