Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Co-expression of xerophyte Zygophyllum xanthoxylum ZxNHX and ZxVP1-1 enhances salt and drought tolerance in transgenic Lotus corniculatus by increasing cations accumulation

Ai-Ke Bao A B , Yan-Wen Wang A B , Jie-Jun Xi A B , Chen Liu A , Jin-Lin Zhang A and Suo-Min Wang A C
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730 020, PR China.

B These authors have contributed equally to this work.

C Corresponding author. Email: smwang@lzu.edu.cn

Functional Plant Biology 41(2) 203-214 https://doi.org/10.1071/FP13106
Submitted: 19 April 2013  Accepted: 15 August 2013   Published: 11 October 2013

Abstract

Lotus corniculatus L. is an important legume for forage, but is sensitive to salinity and drought. To develop salt- and drought-resistant L. corniculatus, ZxNHX and ZxVP1-1 genes encoding tonoplast Na+/H+ antiporter and H+-pyrophosphatase (H+-PPase) from a succulent xerophyte Zygophyllum xanthoxylum L., which is well adapted to arid environments through accumulating Na+ in its leaves, were transferred into this forage. We obtained the transgenic lines co-expressing ZxNHX and ZxVP1-1 genes (VX) as well as expressing ZxVP1-1 gene alone (VP). Compared with wild-type, both VX and VP transgenic lines grew better at 200 mM NaCl, and also exhibited higher tolerance and faster recovery from water-deficit stress: these performances were associated with more Na+, K+ and Ca2+ accumulation in their leaves and roots, which caused lower leaf solute potential and thus retained more water. Moreover, the transgenic lines maintained lower relative membrane permeability and higher net photosynthesis rate under salt or water-deficit stress. These results indicate that expression of tonoplast Na+/H+ antiporter and H+-PPase genes from xerophyte enhanced salt and drought tolerance of L. corniculatus. Furthermore, compared with VP, VX showed higher shoot biomass, more cations accumulation, higher water retention, lesser cell membrane damage and higher photosynthesis capacity under salt or water-deficit condition, suggesting that co-expression of ZxVP1-1 and ZxNHX confers even greater performance to transgenic L. corniculatus than expression of the single ZxVP1-1.

Additional keywords: H+-PPase, tonoplast Na+/H+ antiporter.


References

Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiology 123, 1047–1056.
Ionic and osmotic effects of NaCl induced inactivation of photosystems I and II in Synechococcus sp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Slt74%3D&md5=91bce23da09940fb422f9e2822903e7bCAS | 10889254PubMed |

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.
Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1Sju7s%3D&md5=b02bb3a0e26a6d6e23d1e4d4dc567855CAS | 10455050PubMed |

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. The Plant Journal 36, 229–239.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1OgtLk%3D&md5=577998de8c12babbb465e36914674c1bCAS | 14535887PubMed |

Bao AK, Wang SM, Wu GQ, Xi JJ, Zhang JL, Wang CM (2009) Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant Science 176, 232–240.
Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFagtbvN&md5=0a4aee81c94daa31c9e15b98d86aa9b0CAS |

Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 23–58.
Drought and salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXis12ns7c%3D&md5=aa8bab8304793b0e6dee077dad09bb65CAS |

Bassil E, Tajima H, Liang YC, Ohto M, Ushijim K, Nakano R, Esumi T, Coku A, Belmonte M, Blumwald E (2011) The Arabidopsis Na+/H+ antiporters nhx1 and nhx2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. The Plant Cell 23, 3482–3497.
The Arabidopsis Na+/H+ antiporters nhx1 and nhx2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVGqtrvP&md5=6d0bdc9d7720670a32b1fa1f9be18da7CAS | 21954467PubMed |

Bhaskaran S, Savithramma DL (2011) Co-expression of Pennisetum glaucum vacuolar Na+/H+ antiporter and Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic tomato. Journal of Experimental Botany 62, 5561–5570.
Co-expression of Pennisetum glaucum vacuolar Na+/H+ antiporter and Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFCit7%2FK&md5=a85adebc51ef0d3842489c16d8c383abCAS | 21841179PubMed |

Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmoudi K (2007) Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt-and drought-stress tolerance in Arabidopsis thaliana plants. Journal of Experimental Botany 58, 301–308.
Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt-and drought-stress tolerance in Arabidopsis thaliana plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOltL0%3D&md5=b7b91a614593c5e58efa0cd149a9a5d3CAS | 17229760PubMed |

Chen H, An R, Tang JH, Cui XH, Hao FS, Chen J, Wang XC (2007) Over-expression of a vacuolar Na+/H+ antiporter gene improves salt tolerance in an upland rice. Molecular Breeding 19, 215–225.
Over-expression of a vacuolar Na+/H+ antiporter gene improves salt tolerance in an upland rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhslWjtLY%3D&md5=5ef638d385b4b6b7969fb3858111945dCAS |

Cheng X, Wang YW, Bao AK, Wang SM (2010) Overexpression of AVP1 enhanced salt and drought tolerance of Lotus corniculatus. Plant Physiology Communications 46, 808–816. [In Chinese]

Conn SJ, Gilliham M, Athman A, Schreiber AW, Baumann U, Moller I, Cheng NH, Stancombe MA, Hirschi KD, Webb AAR, Burton R, Kaiser BN, Tyerman SD, Leigh RA (2011) Cell-specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentration, gas exchange, and plant productivity in Arabidopsis. The Plant Cell 23, 240–257.
Cell-specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentration, gas exchange, and plant productivity in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFCmsrs%3D&md5=67e4eb3fafc5096ec7e6da9e9e8de136CAS | 21258004PubMed |

Ferjani A, Segami S, Horiguchi G, Muto Y, Maeshima M, Tsukaya H (2011) Keep an eye on PPi: the vacuolar-type H+-pyrophosphatase regulates postgerminative development in Arabidopsis. The Plant Cell 23, 2895–2908.
Keep an eye on PPi: the vacuolar-type H+-pyrophosphatase regulates postgerminative development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlSqsL%2FE&md5=26a1f63b84bf53bcda0b9d1e794531b0CAS | 21862707PubMed |

Flowers TJ (2004) Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.
Improving crop salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1egtQ%3D%3D&md5=ba62fd0b22f1d3b5393d8ae4f78ee465CAS | 14718494PubMed |

Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Experimental Cell Research 50, 151–158.
Nutrient requirements of suspension cultures of soybean root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXktVyqtLw%3D&md5=2929e479076a4f5626e2363079f2de91CAS | 5650857PubMed |

Gao F, Gao Q, Duan XG, Yue GD, Yang AF, Zhang JR (2006) Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. Journal of Experimental Botany 57, 3259–3270.
Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1ygt7k%3D&md5=7d159069d7d72856db8360b05afdd947CAS | 16940040PubMed |

Gaxiola RA, Rao RI, 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 of the United States of America 96, 1480–1485.
The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1 can function in cation detoxification in yeast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFSru7o%3D&md5=46d34def5ec196454b9c1fe5ed2e82a4CAS | 9990049PubMed |

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. Proceedings of the National Academy of Sciences of the United States of America 98, 11444–11449.
Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1yqurc%3D&md5=72857fc67121f537f9f44c44460c7f7aCAS | 11572991PubMed |

Gaxiola RA, Fink GR, Hirschi KD (2002) Genetic manipulation of vacuolar proton pumps and transporters. Plant Physiology 129, 967–973.
Genetic manipulation of vacuolar proton pumps and transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsFWqur8%3D&md5=c0d0c149525be5cdefefa4edad55dc54CAS | 12114553PubMed |

Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Letters 581, 2204–2214.
Plant proton pumps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1aitbY%3D&md5=54d92eb2524290d70832136180c64961CAS | 17412324PubMed |

Gouiaa S, Khoudi H, Leidi EO, Pardo JM, Masmoudi K (2012) Expression of wheat Na+/H+ antiporter TNHXS1 and H+-pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance. Plant Molecular Biology 79, 137–155.
Expression of wheat Na+/H+ antiporter TNHXS1 and H+-pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFWmtL0%3D&md5=3e96e435f8854be9dd79d003e2e298daCAS | 22415161PubMed |

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.
Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Ons7fN&md5=7fee7ad1576e60c45edc634f795265f3CAS |

Hirschi KD (2004) The calcium conundrum: both versatile nutrient and specific signal. Plant Physiology 136, 2438–2442.
The calcium conundrum: both versatile nutrient and specific signal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOrtb0%3D&md5=e9d8c29a0b40a8cbb816e4107af1bbb8CAS | 15375199PubMed |

Leidi EO, Barragan V, Rubio L, El-Hamdaoui A, Ruiz MT, Cubero B, Fernandez JA, Bressan RA, Hasegawa PM, Quintero FJ, Pardo JM (2010) The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. The Plant Journal 61, 495–506.
The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFGqtL0%3D&md5=68e0881643caf59b4922809d18c09c86CAS | 19912566PubMed |

Li J, Yang H, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek BA, Murphy AS, Gilroy S, Gaxiola RA (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310, 121–125.
Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKqu7fE&md5=2f7f85b4358c977e7457b0492f2ae436CAS | 16210544PubMed |

Li ZG, Baldwin CM, Hu Q, Liu HB, Luo H (2010) Heterologous expression of Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass (Agrostis stolonifera L.). Plant, Cell & Environment 33, 272–289.
Heterologous expression of Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic creeping bentgrass (Agrostis stolonifera L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFKgsr4%3D&md5=5b6cd045e5cd20737655410b63e69d4cCAS |

Liu JQ, Pu JC, Liu XM (1987) Comparative studies on water relations and xeromorphic structures of some plant species in the middle part of the desert zone in China. Acta Botanica Sinica 29, 662–673. [In Chinese]

Liu SP, Zheng LQ, Xue YH, Zhang Q, Wang L, Shou HX (2010) Overexpression of OsVP1 and OsNHX1 increases tolerance to drought and salinity in rice. Journal of Plant Biology 53, 444–452.
Overexpression of OsVP1 and OsNHX1 increases tolerance to drought and salinity in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVeqsr3I&md5=4a9502f0505e1affb3381da5a90622abCAS |

Lv SL, Zhang KW, Gao Q, Lian LJ, Song Y, Zhang J (2008) Overexpression of an H+-PPase gene from Thellungiella halophila (TsVP) in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant & Cell Physiology 49, 1150–1164.
Overexpression of an H+-PPase gene from Thellungiella halophila (TsVP) in cotton enhances salt tolerance and improves growth and photosynthetic performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFSrsbnO&md5=2493598db792aa27ac6d0f13f34f151bCAS |

Lv SL, Lian LJ, Tao PL, Li ZX, Zhang KW, Zhang JR (2009) Overexpression of Thellungiella halophila H+-PPase (TsVP) in cotton enhances drought stress resistance of plants. Planta 229, 899–910.
Overexpression of Thellungiella halophila H+-PPase (TsVP) in cotton enhances drought stress resistance of plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1agsLk%3D&md5=413566cf89b88deab5959a3d6a3d899eCAS | 19130078PubMed |

Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiology 32, 4–13.
Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVCmt7Y%3D&md5=799a0c145cf3d3a4d3d01f99ddc474dbCAS | 21979327PubMed |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=0ce1f7aad22c73fffb329d4603f0e836CAS | 18444910PubMed |

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Physiologia Plantarum 15, 473–497.
A revised medium for rapid growth and bioassays with tobacco cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=00e945f2329f915ef516a05110061063CAS |

Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiology 109, 735–742.

Park S, Li J, Pittman JK, Berkowitz GA, Yang H, Undurraga S, Morris J, Hirschi KD, Gaxiola RA (2005) 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 102, 18830–18835.
Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVyrtw%3D%3D&md5=710d36b66429ae9c536d93cefea08371CAS | 16361442PubMed |

Pasapula V, Shen G, Chen J, Qiu XY, Zhu LF, Zhang XL, Auld D, Blumwald E, Zhang H, Gaxiola RA, Payton P (2011) Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions. Plant Biotechnology Journal 9, 88–99.
Expression of an Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) in cotton improves drought- and salt tolerance and increases fibre yield in the field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOmtbk%3D&md5=3ae7233c3eedc21f76e8d0684e9f288aCAS | 20492547PubMed |

Shabala S (2003) Regulation of potassium transport in leaves: from molecular to tissue level. Annals of Botany 92, 627–634.
Regulation of potassium transport in leaves: from molecular to tissue level.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVOnsbw%3D&md5=15b8b0fc40a9e5f4f4012311ff4cce07CAS | 14500326PubMed |

Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651–669.
Potassium transport and plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Oit70%3D&md5=b00298e506b7189fc2da0a5277d6448aCAS | 18724408PubMed |

Singla-Pareek SL, Reddy MK, Sopory SK (2003) Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. Proceedings of the National Academy of Sciences of the United States of America 100, 14672–14677.
Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvFaqsrg%3D&md5=a06cc8a69fb4c0bf2417abc1cd005c66CAS | 14638937PubMed |

Walker DJ, Leigh RA, Miller AJ (1996) Potassium homeostasis in vacuolate plant cells. Proceedings of the National Academy of Sciences of the United States of America 93, 10510–10514.
Potassium homeostasis in vacuolate plant cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrmtFKhug%3D%3D&md5=a1a22b30105283290233e5c342c2b9deCAS | 11607707PubMed |

Wang SM, Wan CG, Wang YR, Chen H, Zhou ZY, Fu H, Sosebeeb RE (2004) The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China. Journal of Arid Environments 56, 525–539.
The characteristics of Na+, K+ and free proline distribution in several drought-resistant plants of the Alxa Desert, China.Crossref | GoogleScholarGoogle Scholar |

Wu GQ, Xi JJ, Wang Q, Bao AK, Ma Q, Zhang JL, Wang SM (2011) 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 168, 758–767.
The ZxNHX gene encoding tonoplast Na+/H+ antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktFKjt7o%3D&md5=e01116b3c4218fb7fb9e0964981d8962CAS | 21216025PubMed |

Xue ZY, Zhi DY, Xue G, Zhang H, Zhao Y, Xia G (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.
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+.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Wksrs%3D&md5=9d15c0d3c8a300d0cd863b2af01c5ef7CAS |

Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends in Plant Science 10, 615–620.
Developing salt-tolerant crop plants: challenges and opportunities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Oms7%2FI&md5=310049fd20ed5df264f35b9904411c39CAS | 16280254PubMed |

Yue LJ, Li SX, Ma Q, Zhou XR, Wu GQ, Bao AK, Zhang JL, Wang SM (2012) NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum. Journal of Arid Environments 87, 153–160.
NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum.Crossref | GoogleScholarGoogle Scholar |

Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology 19, 765–768.
Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslektLw%3D&md5=160c1b2f69fafc27ca6e47963b22ba74CAS | 11479571PubMed |

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. Proceedings of the National Academy of Sciences of the United States of America 98, 12832–12836.
Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotFahsLs%3D&md5=2ae5dcd60094ddbbcba5ed00f410b2c1CAS | 11606781PubMed |

Zhao FY, Zhang XJ, Li PH, Zhao YX, Zhang H (2006) Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Molecular Breeding 17, 341–353.
Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1.Crossref | GoogleScholarGoogle Scholar |

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247–273.
Salt and drought stress signal transduction in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhtbc%3D&md5=f20f5493d7e57fe0984b2dba9a510739CAS | 12221975PubMed |