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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Improvement of Torenia fournieri salinity tolerance by expression of Arabidopsis AtNHX5

Le-Yi Shi A , Hong-Qing Li B , Xiao-Ping Pan A , Guo-Jiang Wu A and Mei-Ru Li A C
+ Author Affiliations
- Author Affiliations

A South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, People’s Republic of China.

B Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, South China Normal University, Guangzhou 510631, People’s Republic of China.

C Corresponding author. Email: limr@scbg.ac.cn

Functional Plant Biology 35(3) 185-192 https://doi.org/10.1071/FP07269
Submitted: 16 November 2007  Accepted: 11 February 2008   Published: 23 April 2008

Abstract

In this paper, transgenic torenia plants expressing the AtNHX5 gene from Arabidopsis in sense and antisense orientations were produced to examine the potential role of AtNHX5 in plant salt tolerance and development. We found that torenia plants overexpressing AtNHX5 showed markedly enhanced tolerance to salt stress compared with both wild-type and antisense AtNHX5 transgenic plants upon salt stress. Measurements of ion levels indicated that Na+ and K+ contents were all higher in AtNHX5 overexpressing shoots than in those of both wild-type and antisense AtNHX5 shoots treated with 50 mm NaCl. This indicated that overexpression of AtNHX5 could improve the salt tolerance of transgenic torenia via accumulation of both Na+ and K+ in shoots, in which overall ion homeostasis and osmotic adjustment was changed to sustain the increase in shoot salt tolerance. Further, we found that overexpression of AtNHX5 in torenia significantly improved the shoot regeneration frequency in leaf explants and increased the plantlet survival rate when transferring the regenerated plants to soil. In addition, the AtNHX5 expressing plants produced flowers earlier than both wild-type and the antisense AtNHX5 plants. Taken together, the results indicated that AtNHX5 functions not only in plant salt tolerance but also in plant growth and development.

Additional keywords: growth, transgenic plants.


Acknowledgements

This research was supported by the National Natural Science Foundation of China (No. 30170667), the CAS ‘100 Talents’ Program and the Joint Funds of NSFC-Guangdong No. U0731006.


References


Aharon GS, Apse MP, Duan S, Hua X, Blumwald E (2003) Characterization of a family of vacuolar Na+/H+ antiporters in Arabidopsis thaliana. Plant and Soil 253, 245–256.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are related in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. The Plant Journal 36, 229–239.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Blumwald E (2000) Sodium transport and salt tolerant in plants. Current Opinion in Cell Biology 12, 431–434.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Chinnusamy V , Zhu JK (2003) Plant salt tolerance. In ‘Plant responses to abiotic stress’. (Eds H Hirt, K Shinozaki) pp. 241–270. (Springer-Verlag: Berlin)

FAO (2005) Global network on integrated soil management for sustainable use of salt-affected soils. FAO Land and Plant Nutrition Management Service Rome. Italy. Available at http://www.fao.org/ag/agl/agll/spush

Fila G, Ghashghaic J, Hoarau J, Cornic G (1998) Photosynthesis, leaf conductance and water relations of in vitro cultured grapevine rootstock in relation to acclimatization. Physiologia Plantarum 102, 411–418.
Crossref | GoogleScholarGoogle Scholar | open url image1

Flowers TJ (2004) Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

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+ from rice. Plant & Cell Physiology 45, 146–159.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

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. Proceedings of the National Academy of Sciences USA 96, 1480–1485.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants results from overexpression of the AVP1 H+-Pump. Proceedings of the National Academy of Sciences USA 98, 11444–11449.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 Molecular Biology 46, 35–42.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hasegawa PM, Bressan R, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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 Physiology 46, 1848–1854.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Li M-L, Wang X-J, Li H-Q (2006) Establishment of Agrobacterium-mediated transformation system for Torenia. Acta Horticulturae Sinica 33, 105–110. open url image1

Lu SY, Jing YX, Shen SH, Zhao HY, Zhou XJ, Ren Q (2005) Antiporter gene from Hordum brevisubulatum (Trin.) link and its overexpressioin in transgenic tobaccos. Journal of Integrative Plant Biology 47, 343–349.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ma P-K, Jia X-L, Zhang Q-G (2002) Improvement of water use efficiency in winter wheat by breeding lines with low rate of water loss of excised-leaves. Agricultural Sciences in China 12, 1310–1316. open url image1

Muhammad AL, Ye G-N, Weeden NF, Reisch BI (1994) A simple and efficient method for DNA extraction from grapevine cultivars, Vitis species and Ampelopsis. Plant Molecular Biology Reporter 12, 6–13. open url image1

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 241–252. open url image1

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Letters 532, 279–282.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Pardo J, Cubero B, Leidi E, Quintero FJ (2006) Alkali cation exchangers: role in cellular homeostais and stress tolerance. Journal of Experimental Botany 57, 1181–1199.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Porat R, Pavoncello D, Ben-Hayyim G, Lurie S (2002) A heat treatment induced the expression of a Na+/H+ antiport gene (cNHX1) in citrus fruit. Plant Science 162, 957–963.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pospisilova J, Wilhelmova N, Synkova H, Catsky J, Krebs D , et al. (1998) Acclimation of tobacco plantlets to ex vitro conditions as affected by application of abscisic acid. Journal of Experimental Botany 49, 863–869.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pospisilova J, Ticha I, Kadlecek P, Haiedl D, Plzakova S (1999) Acclimatization of micropropagated plants to ex vitro conditions. Biologia Plantarum 42, 481–497.
Crossref | GoogleScholarGoogle Scholar | open url image1

Quintero FJ, Blatt MR, Pardo JM (2000) Functional conservation between yeast and plant endosomal Na+/H+ antiporters. FEBS Letters 471, 224–228.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Rajagopal D, Agarwal P, Tyagi W, Singla-Pareek SL, Reddy MK, Sopory SK (2007) Pennisetum glaucum Na+/H+ antiporter confers high level of salinity tolerance in transgenic Brassica juncea. Molecular Breeding 19, 137–151.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences UAA 97, 6896–6901.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnology 21, 81–85.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Song C-P, Guo Y, Qiu Q, Lambert G, Galbraith DW, Jagendorf A, Zhu J-K (2004) A probable Na+(K+)/H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 101, 10211–10216.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Venema K, Belver A, Marin-Manzano MC, Rodriguez-Rosales MP (2003) A novel intracellular K+/H+ antiporter related to Na+/H+ antiporters is important for K+ ion homeostasis in plants. Journal of Biological Chemistry 278, 22453–22459.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

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. Biologia Plantarum 48, 509–515.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wu CA, Yang GD, Meng QW, Zheng CC (2004) The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ exchanger plays an important role in salt stress. Plant & Cell Physiology 45, 600–605.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Xue Z-Y, Zh D-Y, Xue G-P, Zhang H, Zhao Y-X, Xia G-M (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 Science 167, 849–859.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yamaguchi T, Fukada-Tanaka S, Inagaki Y, Saito N, Yonekura-Sakakibara K, Tanaka Y, Kusumi T, Iida S (2001) Genes encoding the vacuolar Na+/H+ exchanger and flower coloration. Plant & Cell Physiology 42, 451–461.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Yokoi S, Quintero FJ, Cubero B, 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. The Plant Journal 30, 529–539.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Yoshida K, Kawachi M, Mori M, Maeshima M, Kondo M, Nishimura M, Kindo T (2005) Sepal color variation of Hydrangea macrophylla and vacuolar pH measured with a proton-selective microelectrode. Plant & Cell Physiology 46, 407–415.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Zhang H-X, Blumward E (2001) Transgenenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology 19, 765–768.
Crossref | GoogleScholarGoogle Scholar | PubMed | PubMed | open url image1

Zhang H-X, Hodson J, 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. Proceedings of the National Academy of Sciences USA 98, 12832–12836.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology 6, 441–445.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1