Research advances in higher plant adaptation to salt stress

doi:10.11686/cyxb2015233

Abstract

Abstract: Soil salinity is a serious worldwide problem causing reduction in crop growth and agricultural output potential. Consequently, finding new ways to minimize the adverse effects of soil salinization on agriculture is globally important. Understanding the adaptation mechanisms of higher plants to salt stress is critical for enhancing salt tolerance and yields of crop plants as well as protecting ecological environments. In this paper, we reviewed the key progresses in salt stress adaptation of higher plants, including the effects of salt stress in plants; physiological mechanism of plant salt tolerance (osmotic adjustment, nutrient balance and the antioxidant system); the diversity of genes relevant to salt tolerance (ion transporting protein genes, osmotic regulation-related genes, signal transduction-related genes and cellular antioxidant-related genes and so on); and the approaches for crop improvement in salt tolerance. Prospects for developing crop plants tolerant to salinity are also discussed.

ZHANG Jin-Lin, LI Hui-Ru, GUO Shu-Yuan, WANG Suo-Min, SHI Hua-Zhong, HAN Qing-Qing, BAO Ai-Ke, MA Qing. Research advances in higher plant adaptation to salt stress[J]. Acta Prataculturae Sinica, 2015, 24(12): 220-236.

References

[1] Flowers T J. Improving crop salt tolerance. Journal of Experimental Botany, 2004, 55: 307-319.
[2] Kronzucker H J, Coskun D, Schulze L M, et al . Sodium as nutrient and toxicant. Plant and Soil, 2013, 369: 1-23.
[3] Janz D, Polle A. Harnessing salt for woody biomass production. Tree Physiology, 2012, 32: 1-3.
[4] Zhang J L, Flowers T J, Wang S M. Mechanisms of sodium uptake by roots of higher plants. Plant and Soil, 2010, 326: 45-60.
[5] Zhao K F, Li F Z, Fan S J, et al . Halophytes in China. Chinese Bulletin of Botany, 1999, 16(3): 201-207.
[6] Zhao K F. Plants adapt to salt adversity. Bulletin of Biology, 2002, 37(6): 7-10.
[7] Zhang J L, Shi H Z. Physiological and molecular mechanisms of plant salt tolerance. Photosynthesis Research, 2013, 115: 1-22.
[8] Munns R, Tester M. Mechanisms of salinity tolerance. Annual Review of Plant Biology, 2008, 59: 651-681.
[9] Zhu J K. Plant salt tolerance. Trends in Plant Science, 2001, 6: 66-71.
[10] Kronzucker H J, Britto D T. Sodium transport in plants: a critical review. New Phytologist, 2011, 189: 54-81.
[11] Gorai M, El A W, Yang X, et al .Toward understanding the ecological role of mucilage in seed germination of a desert shrub Henophyton deserti : interactive effects of temperature, salinity and osmotic stress. Plant and Soil, 2014, 374: 727-738.
[12] Wei Y, Dong M, Huang Z Y, et al . Factors influencingseed germination of Salsola affinis (Chenopodiaceae), a dominant annual halophyte inhabiting the deserts of Xinjiang. Flora of China, 2008, 203: 134-140.
[13] Li Y, Shen Y Y, Yan S G. Comparative studies of effect of NaCl stress on the seed germination of 5 forage species. Pratacultural Science, 1997, 14(2): 50-53.
[14] Liang Y C. Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress. Plant and Soil, 1999, 209: 217-224.
[15] Trono D, Flagella Z, Laus M N, et al . The uncoupling protein and the potassium channel are activated by hyperosmotic stress in mitochondria from durum wheat seedlings. Plant Cell and Environment, 2004, 27: 437-448.
[16] Becker D, Hoth S, Ache P, et al . Regulation of the ABA-sensitive Arabidopsis potassium channel gene GORK in response to water stress. Febs Letters, 2003, 554: 119-126.
[17] Ottow E A, Brinker M, Teichmann T, et al . Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiology, 2005, 139: 1762-1772.
[18] Song J, Ding X D, Feng G, et al . Nutritional and osmotic roles of nitrate in a euhalophyte and a xerophyte in saline conditions. New Phytologist, 2006, 171: 357-366.
[19] Liu J, Cai H, Liu Y, et al . A study on physiological characteristics and cmparison of salt resistance of two Medicago sativa at the seeding stage. Acta Prataculturae Sinica, 2013, 22(2): 250-256.
[20] Jarunee J, Kenjiusui, Hiroshi M. Differences in physiological responses to NaCl between salt-tolerant Sesbania rostrata Brem.and Obem.And non-tolerant Phaseolus vulgaris L. Weed Biology and Management, 2003, 3: 21-27.
[21] Makela P, Karkkainen J, Somersalo S. Effect of glycinebetaine on chloroplast ultrastructure, chlorophyll and protein content, and RuBPCO activities in tomato grown under drought or salinity. Biologia Plantarum, 2000, 43: 471-475.
[22] Leshem Y, Melamed B N, Cagnac O, et al . Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H 2 O 2 containing vesicles with tonoplast and increased salt tolerance. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103: 18008-18013.
[23] Flowers T J, Colmer T D. Salinity tolerance in halophytes. New Phytologist, 2008, 179: 945-963.
[24] Shabala S, Bose J, Hedrich R. Salt bladders: do they matter. Trends in Plant Science, 2014, 19(11): 687-691.
[25] Wang C M, Zhang J L, Liu X S, et al . Puccinellia tenuiflora maintains a low Na + level under salinity by limiting unidirectional Na + influx resulting in a high selectivity for K + over Na + . Plant, Cell and Environment, 2009, 32: 486-496.
[26] Ueda A, Yamamoto-Yamane Y, Takabe T. Salt stress enhances proline utilization in the apical region of barley roots. Biochemical and Biophysical Research Communications, 2007, 355: 61-66.
[27] Wang C Q, Zhao J Q, Chen M, et al . Identification of betacyanin and effects of environmental factors on its accumulation in halophyte Suaeda salsa . Journal of Plant Physiology and Molecular Biology, 2006, 32(2): 195-201.
[28] Md A H, Mst N A B, Yoshimasa N, et al . Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. Journal of Plant Physiology, 2008, 165: 813-824.
[29] Incharoensakd A, Takabe T, A kazawa T. Effect of bteaine on enzyme activity and subunit internation of ribulose-1,5 -bisphosphate carboxylase/oxygenas from Aphnothece halophytica . Plant Physiology, 1986, 81: 1044-1049.
[30] Dubey R S, Singh A K. Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolising enzymes in rice plants. Biologia Plantarum, 1999, 42: 233-239.
[31] Shabala S, Shabala L. Ion transport and osmotic adjustment in plants and bacteria. Biomolecular Concepts, 2011, 2: 407-419.
[32] Demidchik V, Cuin T A, Svistunenko D, et al . Arabidopsis root K + -efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science, 2010, 123: 1468-1479.
[33] Teaklea N L, Bazihizina N, Shabala S, et al . Differential tolerance to combined salinity and O 2 deficiency in the halophytic grasses Puccinellia ciliata and Thinopyrum ponticum : The importance of K + retention in roots. Environmental and Experimental Botany, 2013, 87: 69-78.
[34] Wang S M, Zhang J L, Flowers T J. Low-affinity Na + uptake in the halophyte Suaeda maritima . Plant Physiology, 2007, 145(2): 559-571.
[35] Cuin T A, Bose J, Stefano G, et al . Assessing the role of root plasma membrane and tonoplast Na + /H + exchangers in salinity tolerance in wheat: in planta quantification methods. Plant, Cell and Environment, 2009, 34: 947-961.
[36] Schmidt U G, Endler A, Schelbert S, et al . Novel tonoplast transporters identified using a proteomic approach with vacuoles isolated from cauliflower buds. Plant Physiology, 2007, 145: 216-229.
[37] Wu G Q, Xi J J, Wang Q, et al . The ZxNHX gene encoding tonoplast Na + /H + antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought. Journal of Plant Physiology, 2011, 168: 758-767.
[38] Ma Q, Yue L J, Zhang J L, et al . Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum . Tree Physiology, 2012, 32(1): 4-13.
[39] Yue L J, Li S X, Ma Q, et al . NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum . Journal of Arid Environments, 2012, 87: 153-160.
[40] Wang S M, Zhu X Y, Shu X X. Studies on the characteristics of ion absorption anddistribution in Puccinellia tenuiflora . Acta Prataculturae Sinica, 1994, 3(1): 39-43.
[41] Guo Q, Meng L, Mao P C, et al . Salt tolerance in two tall wheatgrass species is associated with selective capacity for K + over Na + . Acta Physiologiae Plantarum, 2014, 37:1708.
[42] Zhang J L, Flowers T J, Wang S M. Differentiation of low-affinity Na + uptake pathways and kinetics of the effects of K + on Na + uptake in the halophyte Suaeda maritime . Plant and Soil, 2013, 368(1-2): 629-640.
[43] Zhu Z J, Wei G Q, Li J, et al . Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber ( Cucumis sativus L.). Plant Science, 2004, 167: 527-533.
[44] Liang Y C, Zhang W H, Chen Q, et al . Effects of silicon on H + -ATPase and H + -PPase activity, fatty acid composition and fluidity of tonoplast vesicles from roots of salt-stressed barley ( Hordeum vulgare L.). Environmental and Experimental Botany, 2005, 53: 29-37.
[45] Gong H J, Randall D P, Flowers T J. Silicon deposition in the root reduces sodium uptake in rice ( Oryza sativa L.) seedlings by reducing bypass flow. Plant Cell and Environment, 2006, 29: 1970-1979.
[46] Ma J F, Yamaji N, Mitani N, et al . An efflux transporter of silicon in rice. Nature, 2007, 448: 209-212.
[47] Wang X S, Han J G. Effects of NaCl and silicon on ion distribution in the roots, shoots and leaves of two alfalfa cultivars with different salt tolerance. Soil Science and Plant Nutrition, 2007, 53: 278-285.
[48] Tuna A L, Kaya C, Higgs D, et al . Silicon improves salinity tolerance in wheat plants. Environmental and Experimental Botany, 2008, 62: 10-16.
[49] Chai Q, Shao X, Zhang J. Silicon effects on Poa pratensis responses to salinity. HortScience, 2010, 45: 1876-1881.
[50] Bose J, Rodrigo-Moreno A, Shabala S. ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany, 2014, 65(5): 1241-1257.
[51] Guan B, Yv J B, Lu Z H, et al .Effects of water-salt stresses on seeding growth and activities of antioxidative enzyme of Suaeda salsa in coastal wetlands of the yellow river delta. Environmental Science, 2011, 32(8): 2422-2429.
[52] Lu Y, Lei J Q, Zeng F J, et al . Effects of salt treatments on the growth and ecophysiological characteristies. Acta Prataculturae Sinica, 2014, 23(3): 152-159.
[53] Xue X D, Dong X Y, Duan Y X, et al . A comparison of salt resistance of three kinds of Zoysia at different salt concentrations. Acta Prataculturae Sinica, 2013, 22(6): 315-320.
[54] Ahmed I M, Nadira U A, Bibi N, et al . Secondary metabolism and antioxidants are involved in the tolerance to drought and salinity, separately and combined, in Tibetan wild barley. Environmental and Experimental Botany, 2015, 111: 1-12.
[55] Gao H J, Yang H Y, Bai J P, et al . Ultrastructural and physiological responses of potato ( Solanum tuberosum L.) plantlets to gradient saline stress. Frontiers in Plant Science, 2014, 5: 787.
[56] Talke I N, Blaudez D, Maathuis F J M, et al . CNGCs: prime targets of plant cyclic nucleotide signalling. Trends in Plant Science, 2003, 8: 286-293.
[57] Amtmann A, Sanders D. Mechanism of Na + uptake by plant cells. Advances in Botanical Research, 1999, 29: 75-112.
[58] Tyerman S D, Skerrett I M. Root ion channels and salinity. Scientia Horticulturae, 1999, 78: 175-235.
[59] Zhang H F, Wang S M. Advances in study of Na + uptake and transport in higher plants and Na + homeostasis in the cell. Chinese Bulletin of Botany, 2007, 24(5): 561-571.
[60] Amtmann A, Fischer M, Marsh E L, et al . The wheat cDNA LCT1 generates hypersensitivity to sodium in a salt-sensitive yeast strain. Plant Physiology, 2001, 126: 1061-1071.
[61] Kronzucker H J, Szczerba M W, Schulze L M, et al . Non-reciprocal interactions between K + and Na + ions in barley ( Hordeum vulgare L.). Journal of Experimental Botany, 2008, 59: 2793-2801.
[62] Deinlein U, Stephan A B, Horie T, et al . Plant salt-tolerance mechanisms. Trends in Plant Science, 2014, 19(6): 371-379.
[63] Zamani B M, Ebrahimie E, Niazi A. In silico analysis of high affinity potassium transporter (HKT) isoforms in different plants. Aquatic Biosystems, 2014, 10: 9.
[64] Wang Q, Guan C, Wang P, et al . AtHKT 1;1 and AtHAK 5 mediate low-affinity Na + uptake in Arabidopsis thaliana under mild salt stress. Plant Growth Regulation, 2015, 75(3): 615-623.
[65] Ren Z H, Gao J P, Li L G, et al .A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genetics, 2005, 37: 1141-1146.
[66] Laurie S, Feeney K A, Maathuis F J M, et al . A role for HKT 1 in sodium uptake by wheat roots. Plant Journal, 2002, 32: 139-149.
[67] Kader M A, Seidel T, Golldack D, et al . Expressions of OsHKT 1, OsHKT 2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice ( Oryza sativa L.) cultivars. Journal of Experimental Botany, 2006, 57(15): 4257-4268.
[68] Shao Q, Zhao C, Han N, et al . Cloning and expression pattern of SsHKT 1 encoding a putative cation transporter from halophyte Suaeda salsa . DNA sequence, 2008, 19(2): 106-114.
[69] Senn M E, Rubio F, Banuelos M A, et al . Comparative functional features of plant potassium HvHAK 1 and HvHAK 2 transporters. Journal of Biological Chemistry, 2001, 30: 44563-44569.
[70] Fulgenzi F R, Peralta M L, Mangano S, et al . The ionic environment controls the contribution of the barley HvHAK 1 transporter to potassium acquisition. Plant Physiology, 2008, 147: 252-262.
[71] Carden D E, Walker D J, Flowers T J, et al . Single-cell measurements of the contributions of cytosolic Na + and K + to salt tolerance. Plant Physiology, 2003, 131: 676-683.
[72] Takahashi R, Nishio T, Ichizen N, et al . Cloning and functional analysis of the K + transporter PhaHAK2 from salt-sensitive and salt-tolerant reed plants. Biotechnol Letters, 2007, 29: 501-506.
[73] Golldack D, Quigley F, Michalowski C B, et al .Salinity stress-tolerant and -sensitive rice ( Oryza sativa L.) regulate AKT1-type potassium channel transcripts differently. Plant Molecular Biology, 2003, 51: 71-81.
[74] Kim E J, Kwak J M, Uozumi N, et al . AtKUP 1: An Arabidopsis gene encoding high-affinity potassium transport activity. Plant Cell, 1998, 10: 51-62.
[75] Fu H H, Luan S. AtKUP 1: a dual-affinity K + transporter from Arabidopsis . Plant Cell, 1998, 10: 63-73.
[76] Zhang J L. Low-Affinity Na + Uptake and Accumulation in the Halophyte Suaeda maritina[D]. Lanzhou: Lanzhou University, 2008.
[77] Shi H, Kim Y, Guo Y, et al . The Arabidopsis SOS 5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell, 2003, 15(1): 19-32.
[78] Shi H Z, Quintero F J, Pardo J M, et al . The putative plasma membrane Na + /H + antiporter SOS 1 controls long-distance Na + transport in plants. Plant Cell, 2002, 14: 465-477.
[79] Wu G Q, Wang P, Ma Q, et al . Selective transport capacity for K + over Na + is linked to the expression levels of PtSOS 1 in halophyte Puccinellia tenuiflora . Functional Plant Biology, 2012, 39: 1047-1057.
[80] Liu M, Wang T Z, Zhang W H. Sodium extrusion associated with enhanced expression of SOS 1 underlies different salt tolerance between Medicago falcata and Medicago truncatula seedlings. Environmental and Experimental Botany, 2015, 110: 46-55.
[81] Guo Q, Wang P, Ma Q, et al .Selective transport capacity for K + over Na + is linked to the expression levels of PtSOS 1 in halophyte Puccinellia tenuiflora . Functional Plant Biology, 2012, 39: 1047-1057.
[82] Ma Q, Li Y X, Yuan H J, et al . ZxSOS 1 is essential for long-distance transport and spatial distribution of Na + and K + in the xerophyte Zygophyllum xanthoxylum . Plant and Soil, 2014, 374: 661-676.
[83] Feki K, Quintero F J, Khoudi H, et al . A constitutively active form of a durum wheat Na + /H + antiporter SOS 1 confers high salt tolerance to transgenic Arabidopsis . Plant Cell Reports, 2014, 33(2): 277-288.
[84] Nie W X, Xu L, Yu B J. A putative soybean GmsSOS 1 confers enhanced salt tolerance to transgenic Arabidopsis sos 1-1 mutant. Protoplasma, 2015, 252(1): 127-134.
[85] Ishitani M, Liu J, Halfter U, et al . SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell, 2000, 12(9): 1667-1678.
[86] Martinez-Atienza J, Jiang X, Garciadeblas B, et al . Conservation of the salt overly sensitive pathway in rice. Plant Physiology, 2007, 143: 1001-1012.
[87] Gaxiola R A, Rao R, Sherman A, et al . The Arabidopsis thaliana proton transporters, AtNHX1 and AVP1, can function in cation detoxification in yeast. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96: 1480-1485.
[88] Apse M P, Aharon G S, Snedden W A, et al . Salt tolerance confermi by over expression of a vacuolar NaCMC antiport in Arabidopsis . Science, 1999, 285(12): 1256-1258.
[89] Venema K, Quintero F J, Pardo J M, et al . The Arabidopsis Na + /H + exchanger catalyzes low affinity Na + and K + transport in reconstituted vesicles. Journal of Biological Chemistry, 2002, 277: 2413-2418.
[90] Yamaguchi T, Fukuda-Tanaka S, Inagaki Y, et al . Genes encoding the vacuolar Na + /H + exchanger and flower coloration. Plant Cell Physiology, 2001, 142: 451-461.
[91] Sottosanto J B, Gelli A, Blumwald E. DNA array analyses of Arabidopsis thaliana lacking a vacuolar Na + /H + antiporter: impact of AtNHX1 on gene expression. Plant Journal, 2004, 40: 752-771.
[92] Fukuda A, Nakamura A, Tanaka Y. Molecular cloning and expression of the Na + /H + exchanger gene in Oryza sativa . BBA-Gene Structure and Expression, 1999, 1446: 149-155.
[93] Ohta M, Hayashi Y, Nakashima A, et al . Introduction of a Na + /H + antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Letters, 2002, 532: 279-282.
[94] Fukuda A, Chiba K, Maeda M, et al . Effect of salt and osmotic stresses on the expression of genes for the vacuolar H + -pyrophosphatase, H + -ATPase subunitA, and Na + /H + antiporter from barley. Journal of Experimental Botany, 2004, 55: 585-594.
[95] Wu C A, Yang G D, Meng Q W, et al . The cotton GhNHX 1 gene encoding a novel putative tonoplast Na + /H + antiporter plays an important role in salt stress. Plant Cell Physiology, 2004, 45: 600-607.
[96] Zorb C, Noll A, Karl S, et al . Molecular characterization of Na + /H + antiporters ( ZmNHX ) of maize ( Zea mays L.) and their expression under salt stress. Journal of Plant Physiology, 2005, 162: 55-66.
[97] Brini F, Gaxiola R A, Berkowitz G A, et al . Cloning and characterization of a wheat vacuolar cation/proton antiporter and pyrophosphatase proton pump. Plant Physiology and Biochemistry, 2005, 43:347-354.
[98] Yu J N, Huang J, Wang Z M, et al . An Na + /H + antiporter gene from wheat plays an important role in stress tolerance. Journal of Biosciences, 2007, 32: 1153-1161.
[99] Yang Q C, Wu M S, Wang P Q, et al . Cloning and expression analysis of a vacuolar Na + /H + antiporter gene from alfalfa. DNA sequece, 2005, 16: 352-357.
[100] Li W Y, Wong F L, Tsai S N, et al . Tonoplast-located GmCLC 1 and GmNHX 1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY)-2cells. Plant, Cell and Environment, 2006, 29: 1122-1137.
[101] Qiao W H, Zhao X Y, Li W, et al . Overexpression of AeNHX 1, a root-specific vacuolar Na + /H + antiporter from Agropyron elongatum , confers salt tolerance to Arabidopsis and Festuca plants. Plant Cell Reports, 2007, 26: 1663-1672.
[102] Verma D, Singla-Pareek S L, Rajagopal D, et al . Functional validation of a novel isoform of Na + /H + antiporter from Pennisetum glaucum for enhancing salinity tolerance in rice. Journal of Biosciences, 2007, 32: 621-628.
[103] Li J Y, He X W, Xu L, et al . Molecular and functional comparisons of the vacuolar Na + /H + exchangers originated from glycophytic and halophytic species. Journal of Zhejiang University Science, 2008, 9: 132-140.
[104] Ye C Y, Zhang H C, Chen J H, et al . Molecular characterization of putative vacuolar NHX-type Na + /H + exchanger genes from the salt-resistant tree Populus euphratica . Physiologia Plantarum, 2009, 137: 166-174.
[105] Guan B, Hu Y, Zeng Y, et al . Molecular characterization and functional analysis of a vacuolar Na + /H + antiporter gene ( HcNHX 1) from Halostachys caspica . Molecular Biology Reports, 2010, 38: 1889-1899.
[106] Jha A, Joshi M, Yadav N, et al . Cloning and characterization of the Salicornia brachiata Na + /H + antiporter gene SbNHX 1 and its expression by abiotic stress. Molecular Biology Reports, 2011, 38: 1965-1973.
[107] Liu L, Zeng Y, Pan X, et al . Isolation, molecular characterization, and functional analysis of the vacuolar Na + / H + antiporter genes from the halophyte Karelinia caspica . Molecular Biology Reports, 2012, 39: 7193-7202.
[108] Yuan H J, Ma Q, Wu G Q, et al . ZxNHX controls Na + and K + homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedbackregulation of the expression of genes involved in their transport. Annals of Botany, 2015, 115(3): 495-507.
[109] Yin X Y, Yang A F, Zhang K W, et al . Production and analysis of transgenic maize with improved salt tolerance by the introduction of AtNHX 1 gene. Acta Botanica Sinica, 2004, 46: 854-861.
[110] Xue Z Y, Zhi D Y, Xue G, et al . 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, 2004, 167: 849-859.
[111] He C, Yan J, Shen G, et al . 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, 2005, 46: 1848-1854.
[112] Banjara M, Zhu L, Shen G, et al . Expression of an Arabidopsis sodium/proton antiporter gene ( AtNHX 1) in peanut to improve salt tolerance. Plant Biotechnology Reports, 2012, 6: 59-67.
[113] Rajagopal D, Agarwal P, Tyagi W, et al . Pennisetum glaucum Na + /H + antiporter confers high level of salinity tolerance in transgenic Brassica Juncea . Molecular Breeding, 2007, 19: 137-151.
[114] Shi L Y, Li H Q, Pan X P, et al . Improvement of Torenia fournieri salinity tolerance by expression of Arabidopsis AtNHX 5. Functional Plant Biology, 2008, 35: 185-192.
[115] Zhang G H, Su Q, An L J, et al . Characterization and expression of a vacuolar Na + /H + antiporter gene from the monocot halophyte Aeluropus littoralis . Plant Physiology and Biochemistry, 2008, 46: 117-126.
[116] Zhang Y M, Liu Z H, Wen Z Y, et al . The vacuolar Na + -H + antiport gene TaNHX 2 confers salt tolerance on transgenic alfalfa ( Medicago sativa ). Functional Plant Biology, 2012, 39: 708-716.
[117] Joshi M, Jha A, Mishra A, et al . Developing transgenic Jatropha using the SbNHX 1 gene from an extreme halophyte for cultivation in saline wasteland. PLoS One, 2013, 8(8): e71136.
[118] Mishra S, Alavilli H, Lee B H, et al . Cloning and functional characterization of a vacuolar Na + /H + antiporter gene from mungbean ( VrNHX 1) and its ectopic expression enhanced salt tolerance in Arabidopsis thaliana . PLoS One, 2014, 9(10): e106678.
[119] Sarafian V, Kim Y, Poole R J, et al . Molecular cloning and sequence of cDNA encoding the pyrophosphate-energized vacuolar membrance proton pump of Arabidopsis thaliana . Proceedings of the National Academy of Sciences of the United States of America, 1992, 89: 1775-1779.
[120] Gaxiola R A, Palmgren M G, Schumacher K. Plant proton pumps. FEBS Letters, 2007, 581: 2204-2214.
[121] Gao F, Gao Q, Duan X G, et al . Cloning of an H + -PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. Journal of Experimental Botany, 2006, 57: 3259-3270.
[122] Guo S L, Yin H B, Zhang X, et al . Molecular cloning and characterization of a vacuolar H + -pyrophosphatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis . Plant Molecular Biology, 2006, 60: 41-50.
[123] Li J, Yang H, Peer W A, et al . Arabidopsis H + -PPase AVP 1 regulates auxin-mediated organ development. Science, 2005, 310: 121-125.
[124] Park S, Li J, Pittman J K, et al . Up-regulation of a H + - pyrophosphatase (H + -PPase) as a strategy to engineer drought-resistant crop plants. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102: 18830-18835.
[125] Bao A K, Wang S M, Wu G Q, et al . Overexpression of the Arabidopsis H + -PPase enhanced resistance to salt and drought stress in transgenic alfalfa ( Medicago sativa L.). Plant Science, 2009, 176: 232-240.
[126] Li Z G, Baldwin M, Hu Q, et al . Heterologous expression of Arabidopsis H + -pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass ( Agrostis stolonifera L.). Plant Cell Environment, 2010, 33: 272-289.
[127] Schilling R K, Marschner P, Shavrukov Y, et al . Expression of the Arabidopsis vacuolar H + -pyrophosphatase gene ( AVP 1) improves the shoot biomass of transgenic barley and increases grain yield in a saline field. Plant Biotechnology Journal, 2014, 12(3): 378-386.
[128] Kumar T, Uzma, Khan M R, et al . Genetic improvement of sugarcane for drought and salinity stress tolerance using Arabidopsis vacuolar pyrophosphatase ( AVP 1) gene. Molecular Biotechnology, 2014, 56(3): 199-209.
[129] Lv S L, Lian L J, Tao P L, et al . Overexpression of Thellungiella halophila H + -PPase ( TsVP ) in cotton enhances drought stress resistance of plants. Planta, 2009, 229: 899-910.
[130] Pei L, Wang J, Li K, et al . Overexpression of Thellungiella halophila H + -pyrophosphatase gene improves low phosphate tolerance in maize. PLOS One, 2012, 7(8): e43501.
[131] Yao M, Zeng Y, Liu L, et al . Overexpression of the halophyte Kalidium foliatum H + -pyrophosphatase gene confers salt and drought tolerance in Arabidopsis thaliana . Molecular Biology Reports, 2012, 39: 7989-7996.
[132] Khoudi H, Maatar Y, Gouiaa S, et al . Transgenic tobacco plants expressing ectopically wheat H + -pyrophosphatase (H + -PPase) gene TaVP 1 show enhanced accumulation and tolerance to cadmium. Journal of Plant Physiology, 2012, 169: 98-103.
[133] Li X, Guo C, Gu J, et al . Overexpression of VP, a vacuolar H + -pyrophosphatase gene in wheat ( Triticum aestivum L.), improves tobacco plant growth under Pi and N deprivation, high salinity, and drought. The Journal of Experimental Botany, 2014, 65(2): 683-696.
[134] Zhao F Y, Zhang X J, Li P H, et al . Co-expression of the Suaeda salsa SsNHX 1 and Arabidopsis AVP 1 confer greater salt tolerance to transgenic rice than the single SsNHX 1. Molecular Breeding, 2006, 17: 341-353.
[135] Liu S P, Zheng L Q, Xue Y H, et al . Overexpression of OsVP 1 and OsNHX 1 increases tolerance to drought and salinity in rice. Journal of Integrative Plant Biology, 2010, 53: 444-452.
[136] Brini F, Hanin M, Mezghani I, et al . Overexpression of wheat Na + /H + antiporter TNHX 1 and H + - pyrophosphatase TVP 1 improve salt- and drought-stress tolerance in Arabidopsis thaliana plants. Journal of Experimental Botany, 2007, 58: 301-308.
[137] Bhaskaran S, Savithramma D L. Co-expression of Pennisetum glaucum vacuolar Na + /H + antiporter and Arabidopsis H + - pyrophosphatase enhances salt tolerance in transgenic tomato. Journal of Experimental Botany, 2011, 62: 5561-5570.
[138] Gouiaa S, Khoudi H, Leidi E O, et al . Expression of wheat Na + /H + antiporter TNHXS 1 and H + - pyrophosphatase TVP 1 genes in tobacco from a bicistronictranscriptional unit improves salt tolerance. Plant Molecular Biology, 2012, 79: 137-155.
[139] Bao A K, Wang Y W, Xi J J, et al . Co-expression of xerophyte Zygophyllum xanthoxylum ZxNHX and ZxVP 1-1 enhances salt and drought tolerance in transgenic Lotus corniculatus by increasing cations accumulation. Functional Plant Biology, 2014, 41: 203-214.
[140] Hu L, Lu H, Liu Q L, et al . Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiology, 2005, 25: 1273-1281.
[141] Liu Y, Wang G Y, Liu J J, et al . Transfer of E. coli gutD gene into maize and regeneration of salt-tolerant transgenic plants. Science in China Series C-Life Science, 1999, 42(1): 90-95.
[142] Wang H Z, Huang D N, Lu R F, et al . Salt tolerance of transgenic rice ( Oryza sativa L.) with mtlD gene and gutD gene. Chinese Science Bulletin, 2000, 45: 1685-1690.
[143] Kishor P B K, Hong Z, Mian G H. Over expression of △’-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology, 1995, 108: 1387-1394.
[144] Dure L, Greenway S C, Galau G A. Developmental biochemistry of cottonseed embryogenesis and germination-changing messenger ribonucleic-acid populations as shown by in vitro and in vivo protein-synthesis. Biochemistry, 1981, 20(14): 4162-4168.
[145] Xu D, Duan X, Wang B, et al . Expression of a late embryogenesis abundant protein gene HVA 1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiology, 1996, 110: 249-257.
[146] Zhang N, Wang D, Si H J. Isolation and induced expression of betaine aldehyde dehydrogenase genefrom spinach. Journal of Agricultural Biotechnology, 2004, 12(5): 612-613.
[147] Jia G X, Zhu Z Q, Chang F Q, et al . Transformation of tomato with the BADH gene from Atriplex improves salt tolerance. Plant Cell Reports, 2002, 21(2): 141-146.
[148] Tang N, Zhang H, Li X H, et al . Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiology, 2012, 158: 1755-1768.
[149] Shinozaki K, Yamaguchi-Shinozaki K. Gene expression and signal transduction in water stress response. Plant Physiology, 1997, 115: 327-334.
[150] Wu H J, Zhang Z H, Wang J Y, et al . Insights into salt tolerance from the genome of Thellungiella salsuginea . Proceedings of the National Academy of Sciences, 2012, 109(30): 12219-12224.
[151] Taji T, Seki M, Satou M, et al . Comparative genomics in salt tolerance between Arabidopsis and a Rabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiology, 2004, 135: 1697-1709.
[152] Sheen J. Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiology, 2001, 127: 1466-1475.
[153] Moon H, Lee B, Choi G, et al . NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular reduxstate and enhances multiple stress tolerance in transgenic plants. Proceedings of the National Academy of Sciences, 2003, 100(1): 358-363.
[154] Xie T, Ren R, Zhang Y Y, et al . Molecular mechanism for inhibition of a critical component in the Arabidopsis thaliana abscisic acid signal transduction pathways, SnRK2.6, by protein phosphatase ABI 1. Journal of Biological Chemistry, 2012, 287: 794-802.
[155] Li R F, Zhang J W, Wu G Y, et al . HbCIPK2, a novel CBL-interacting protein kinase from halophyte Hordeum brevisubulatum , confers salt and osmotic stress tolerance. Plant, Cell and Environment, 2012, 35: 1582-1600.
[156] Zhang Q, Lin F, Mao T, et al . Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis . Plant Cell, 2012, 24: 4555-4576.
[157] Roxas V P, Lodhi S A, Garrett D K, et al . Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant & Cell Physiology, 2000, 41(11): 1229-1234.
[158] Kovtun Y, Chiu W L, Tena G, et al . Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97: 2940-2945.
[159] Zhang Z, Wang J, Zhang R X, et al . The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis . The Plant Journal, 2012, 71: 273-287.
[160] Ge Y, Gao P, Xia J Z, et al . The effects of calcium chloride on improving te salt resistance of Zea mays L. Journal of Northeast Agicultural University, 2004, 35(3): 281-284.
[161] Zhang L X, Chang Q S, Hou X G, et al . Effects of sodium salt stress on seed germination of Prunella vulgaris . Acta Prataculturae Sinica, 2015, 24(3): 177-186.
[162] Qian Q, Qu L J, Yuan M, et al .Research advances on plant science in China in 2012. Chinese Bulletin of Botany, 2013, 48: 231-287.
[163] Galvan-Ampudia C S, Testerink C. Salt stress signals shape the plant root. Current Opinion in Plant Biology, 2011, 14: 296-302.
[164] Brady S M, Sarkar S F, Bonetta D, et al . The abscisic acid insensitive 3( ABI 3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis . Plant Journal, 2003, 34: 67-75.
[165] An J P, Chen K S. The relations between the injury of plasma membrane and the increase of aba content in wheat leaves. Jo