Abstract
Drought and salinity are major abiotic stresses affecting rice production. To improve plant tolerance to salinity and drought, we overexpressed rice Na+/H+ exchangers (OsNHX1) and H+-pyrophosphatase in tonoplasts (OsVP1) in a japonica elite rice cultivar, Zhonghua 11. Compared with our wild-type control, transgenic plants overexpressing both genes incurred less damage when exposed to long-term treatment with 100 mM NaCl or water deprivation. Under high-saline conditions, the transformants accumulated less Na+ and malondialdehyde in the leaves, thereby allowing the plants to maintain a low level of leaf water potential and reduce stress-induced damage. Those transgenics also had higher photosynthetic activity during the stress period. Under those conditions, they also showed an increase in root biomass, which enabled more water uptake. These results suggest that OsVP1 and OsNHX1 improve the tolerance of rice crops against drought and salt by employing multiple strategies in addition to osmotic regulation.
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Abbreviations
- DO:
-
Double overexpression
- NHX1:
-
Na+/H+ exchanger 1
- RWC:
-
Relative water content
- WT:
-
Wild type
- VP (V-PPase):
-
Vacuolar H+-pyrophosphatase
References
Allakhverdiev SI, Nishiyama Y, Suzuki I, Tasaka Y, Murata N (1999) Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. Proc Natl Acad Sci USA 96:5862–5867
Allakhverdiev SI, Sakamoto A, Nishiyama Y, Murata N (2000) Inactivation of photosystems I and II in response to osmotic stress in Synechoccus: contribution of water channels. Plant Physiol 122:1201–1208
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
Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36:229–239
Barklaz BJ, Zingarelli L, Blumwald E, Smith JAC (1995) Tonoplast Na+/H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum. Plant Physiol 109:549–556
Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmou K (2007) Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt- and drought-stress tolerance in Arabidopsis thaliana plants. J Exp Bot 58:301–308
Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319
Frame BR, Shou HX, Chikwamba RK, Zhang ZY, Xiang CB, Fonger TM, Pegg SE, Li BC, Nettleton DS, Pei DQ, Wang K (2002) Agrobacterium tumefaciens-mediated transformation of maize embryos using a standard binary vector system. Plant Physiol 129:13–22
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
Gao XH, Ren ZH, Zhao YX, Zhang H (2003) Overexpression of SOD2 increases salt tolerance of Arabidopsis. Plant Physiol 133:1873–1881
Gaxiola RA, Rao R, Sherman A, Grisa 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
Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449
Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992
Hunter CJ, Bianchi S, Cheng P, Muldrew K (2007) Osmoregulatory function of large vacuoles found in notochordal cells of the intervertebral disc. Mol Cell Biomech 4:227–237
Li J, Yang HB, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek B, Murphy AS, Gilroy S, Gaxiola R (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310:121–125
Ma XL, Zhang Q, Shi HZ, Zhu JK, Zhao YX, Ma CL, Zhang H (2004) Molecular cloning and different expression of a vacuolar Na+/H+ antiporter gene in Suaeda salsa under salt stress. Biol Plant 48:219–225
Mittova V, Guy M, Tal M, Volokita M (2004) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55(399):1105–1113
Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon rich regions of the genome. Plant Cell 15:1771–1780
Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK (2002) Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the codA gene are highly tolerant to salt stress. Theor Appl Genet 106:51–57
Muehlbauer FJ, Cho S, Sarker A, McPhee KE, Coyne CJ, Rajesh PN, Ford R (2006) Application of biotechnology in breeding lentil for resistance to biotic and abiotic stress. Euphytica 147:149–165
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109:735–742
Ohta M, Hayashi Y, Nakashima A, Hamada A, Tanaka A, Nakamura T, Hayakawa T (2002) Introduction of a Na+/H+antiporter gene from Atriplex gemelini confers salt tolerance to rice. FEBS Lett 532:279–282
Park S, Li JS, Pittman JK, Berkowitz GA, Yang HB, Undurraga S, Morris J, Hirschi KD, Gaxiola R (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci USA 102:18830–18835
Peever TL, Higgins J (1989) Electrolyte leakage, lipoxygenase and lipid peroxidation induced in tomato leaf tissue by specific and non-specific elicitors from Cladosporium fulvum. Plant Physiol 90:867–875
Qian Q, Seiji Y, Teng S, Zeng DL, Zhu LH, Chen SY (2003) Isolation, expression characteristics and chromosomal locations of three cDNA fragments under salt stress in rice. Acta Bot Sin 45:1090–1095
Shi H, Lee B, Wu S, Zhu J (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85
Shou H, Bordallo P, Wang K (2004) Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize. J Exp Bot 55:1013–1019
Sreenivasulu N, Sopory SK, Kavi Kishor PB (2007) Deciphering the regulatory mechanisms of abiotic stress tolerance in plants by genomic approaches. Gene 388:1–13
Wang BS, Lüttge U, Rataj 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
Xue ZY, Zhi D, Xue GP, Zhang H, Zhao YX, Xia GM (2004) Enhanced salt tolerance of transgenic wheat (Triticum 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
Zhang HX, Blumwald E (2001) Transgenic salt tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768
Zhang HX, 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. Proc Natl Acad Sci USA 98:12832–12836
Zhang JZ, Creelman RC, Zhu JX (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crop plants. Plant Physiol 135:615–621
Zhao F, Zhang X, Li P, Zhao Y, Zhang H (2006) Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Mol Breed 17:341–353
Zhu J (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Acknowledgments
This work was supported by the National High Technology Research and Development Program (2007AA021403), the Specialized Research Fund for the Doctoral Program of China Higher Education (grant no. 20070335081), and the Research Foundation for Talented Scholars in China Three Gorges University (KJ2009B047).
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Liu, S., Zheng, L., Xue, Y. et al. Overexpression of OsVP1 and OsNHX1 Increases Tolerance to Drought and Salinity in Rice. J. Plant Biol. 53, 444–452 (2010). https://doi.org/10.1007/s12374-010-9135-6
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DOI: https://doi.org/10.1007/s12374-010-9135-6