The continuous accumulation of Na+ in detached leaf sections is associated with over-expression of NTHK1 and salt tolerance in poplar plants
Ying Zhang A B , Ying-Xia Yang A , Xiangming Zhou A , Yan-Hong Jia A , Li-Li Nie A , Yue Zhang A , Shou-Yi Chen C , Jing-An Wang B D and Zhong-Qi Liu A D
+ Author Affiliations
- Author Affiliations
A Tianjin Research Center of Agricultural Biotechnology, Tianjin 300192, China.
B College of Life Sciences, Tianjin Normal University, Tianjin 300384, China.
C Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
D Corresponding authors. Emails: zqliu733@yahoo.com.cn, jinganwang899@126.com
Functional Plant Biology 38(3) 236-245 https://doi.org/10.1071/FP10215
Submitted: 15 November 2010 Accepted: 23 January 2011 Published: 29 March 2011
Abstract
Detached leaf sections (2 × 2 cm2) from transgenic poplar line 18-1 and its wild type (WT) (Populus × euramericana ‘Neva’) were used to test their salt tolerance and gene expression under controlled environment conditions. The sections from line 18-1 displayed better tolerance to NaCl stress, indicated by high chlorophyll retention and K+ content but low relative electrolyte leakage (REL). Transient overexpression of NTHK1 (Nicotiana tabacum histidine kinase 1) and V-H+-PPase was found in the detached young leaves from line 18-1 after they had been stressed for a few minutes. The activities of vacuolar-type H+-ATPase and H+-PPase in line 18-1 were boosted initially and then decreased to normal level as in unstressed leaves. After sections were stressed for 10 days, the maximal Na+ concentration in line 18-1 was much higher than that in the WT. The higher capacity for Na+ accumulation in line 18-1 may be due to stable Na+ sequestration into the vacuoles. Osmotic stress imposed little effect on REL and chlorophyll content of the sections. The capacity of detached leaf sections in NaCl solution to tolerate stress and to accumulate Na+ may be useful for identifying genotypes with good salt tolerance in poplar and other plants.
Additional keywords: detached leaf sections, gene expression, Na+ accumulation, V-H+-ATPase, V-H+-PPase.
References
Achard P, Cheng H, DeGrrauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activatated phytohormonal signals. Science 311, 91–94.| Integration of plant responses to environmentally activatated phytohormonal signals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1egtw%3D%3D&md5=a18bf91250cd8dcc8eead31df2e8ef56CAS | 16400150PubMed |
Allen JA, Chambers JL, Stine M (1994) Prospects for increasing the salt tolerance of forest trees: a review. Tree Physiology 14, 843–853.
Apse M, Aharon G, Sneddon W, 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=100b7d568c0a92daa4d1ac981ff7c856CAS | 10455050PubMed |
Ben-Gal A, Borochov-Neori H, Yermiyahu U, Shani U (2009) Is osmotic potential a more appropriate property than electrical conductivity for evaluating whole plant response to salinity? Environmental and Experimental Botany 65, 232–237.
| Is osmotic potential a more appropriate property than electrical conductivity for evaluating whole plant response to salinity?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlKqtr0%3D&md5=f275339c616f1caf14af0f6d4d56bdf1CAS |
Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annual Review of Cell and Developmental Biology 16, 1–18.
| Ethylene: a gaseous signal molecule in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpvFOj&md5=2d820abafd58bb990b21a29b7fc16b82CAS | 11031228PubMed |
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochimica et Biophysica Acta 1465, 140–151.
| Sodium transport in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1Wgtrs%3D&md5=4869d498632435d99e8e27983307a5c7CAS | 10748251PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=606a1898fb14c5ab3908d2f4fe5a0f08CAS | 942051PubMed |
Brini F, Hanin M, Meaghani 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=f0259210c14132488241741e60b7b659CAS | 17229760PubMed |
Cao WH, Liu J, Zhou QY, Cao YR, Zhang SF, Du BX, Zhang JS, Chen SY (2006) Expression of tobacco ethylene receptor NTHK1 alters plant responses to salt stress. Plant, Cell & Environment 29, 1210–1219.
| Expression of tobacco ethylene receptor NTHK1 alters plant responses to salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVCqu7Y%3D&md5=09c3b9c04da01d5bd53656dd3923b5bbCAS | 17080944PubMed |
Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiology 143, 707–719.
| Modulation of ethylene responses affects plant salt-stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvFWnsb0%3D&md5=c2c6fd4eca5c9dec1f2317f43c3f8340CAS | 17189334PubMed |
Chang C, Bleecker AB (2004) Ethylene biology. More than a gas. Plant Physiology 136, 2895–2899.
| Ethylene biology. More than a gas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVynurY%3D&md5=d1ad98139a0ae372dde5c8918bb3bca5CAS | 15489282PubMed |
Chen YF, Etheridge N, Schaller E (2005a) Ethylene signal transduction. Annals of Botany 95, 901–915.
| Ethylene signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVWqtL8%3D&md5=910912536e3875432becce79db168b49CAS | 15753119PubMed |
Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005b) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant, Cell & Environment 28, 1230–1246.
| Screening plants for salt tolerance by measuring K+ flux: a case study for barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGitbnE&md5=f6b7e77c8a03d308a7e9fe5b24d509a3CAS |
Chen ZH, Zhou MX, Newman IA, Mendham NJ, Zhang GP, Shabala S (2007) Potassium and sodium relations in salinized barley tissues as a basis of differential salt tolerance. Functional Plant Biology 34, 150–162.
| Potassium and sodium relations in salinized barley tissues as a basis of differential salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1yqsbk%3D&md5=dcbb031daea72ae368aec0120359b581CAS |
Cuartero J, Bolarin MC, Asins MJ, Mormeno V (2006) Increasing salt tolerance in the tomato. Journal of Experimental Botany 57, 1045–1058.
| Increasing salt tolerance in the tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Glsrc%3D&md5=186f3000496971607c982957dd841797CAS | 16520333PubMed |
Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. Journal of Experimental Botany 59, 2697–2706.
| A root’s ability to retain K+ correlates with salt tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1WisLg%3D&md5=d32fd3cea73b4fa4a2e7020a4bdbe58cCAS | 18495637PubMed |
Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochlan LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proceedings of the National Academy of Sciences of the United States of America 99, 15898–15903.
| Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1egur4%3D&md5=28e62deb126e68262b9c507961b44266CAS | 12456878PubMed |
Garthwaite AJ, Bothmer R, Colmer TD (2005) Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl– into the shoots. Journal of Experimental Botany 56, 2365–2378.
| Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl– into the shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVahtLvJ&md5=d8dfc90c7b0818f0d809e2a263a66150CAS | 16014366PubMed |
Gaxiola RA, Li J, Undurraga S, Dang V, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants resulted 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 resulted from overexpression of the AVP1 H+-pump.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1yqurc%3D&md5=92594053cacd770320d61169f986edffCAS | 11572991PubMed |
Gevaudant F, Duby G, Stedingk E, Zhao R (2007) Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance. Plant Physiology 144, 1763–1776.
| Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgsrs%3D&md5=a3f5cbd10feec910860bce8b98f481e2CAS | 17600134PubMed |
Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Current Opinion in Plant Biology 7, 40–49.
| The ethylene signaling pathway: new insights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFWqtg%3D%3D&md5=695b9893331898db04f58906394bc490CAS | 14732440PubMed |
Hasegawa PM, Bressan RA, 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.
| Plant cellular and molecular responses to high salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymt7s%3D&md5=6cb239a13a0581221e65204097647e08CAS | 15012199PubMed |
He SJ, Zhang JS, Chen SY (2004) Studies on the transformation of NTHK1 in poplar and its salt tolerance. In ‘4th Symposium on Plant Molecular Breeding in China’, p. 86. (Hainan Press: Haikou, China)
Klahn S, Marquardt DM, Rollwitz I, Hagemann M (2009) Expression of ggpPS gene for glucosylglycerol biosynthesis from Azotobacter vinelandii improves the salt tolerance of Arabidopsis thaliana. Journal of Experimental Botany 60, 1679–1689.
| Expression of ggpPS gene for glucosylglycerol biosynthesis from Azotobacter vinelandii improves the salt tolerance of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 19363207PubMed |
Li Y, Su X, Zhang B, Huang Q, Zhang X, Huang R (2009) Expression of jasmonic ethylene responsive factor gene in transgenic poplar tree leads to increased salt tolerance. Tree Physiology 29, 273–279.
| Expression of jasmonic ethylene responsive factor gene in transgenic poplar tree leads to increased salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjtVyjt7g%3D&md5=71141c2490cc7dfd8ff0a302b4440a57CAS | 19203952PubMed |
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 Physiology 49, 1150–1164.
| Overexpression of an H+-PPase gene from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFSrsbnO&md5=270e7201b935c93dbe9b29bc3c62aa35CAS | 18550626PubMed |
Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+ : Na+ ratios. Annals of Botany 84, 123–133.
| K+ nutrition and Na+ toxicity: the basis of cellular K+ : Na+ ratios.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVCgtL4%3D&md5=6a8b3acc292f331f42fa2dc461ee591aCAS |
Morgan PW, Drew MC (1997) Ethylene and plant responses to stress. Physiologia Plantarum 100, 620–630.
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=4ff74227fb3898bf12208db44bd191acCAS | 18444910PubMed |
Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025–1043.
| Approaches to increasing the salt tolerance of wheat and other cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1GlsrY%3D&md5=2be953ee503ac09a2f95e120529424edCAS | 16510517PubMed |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bioassays with tobacco tissue culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=06c472aaff717f5157aa29da67ee5ad0CAS |
Ougham H, Hortenstainer S, Armstead I, Donnison I, King I, Thomas H, Mur L (2008) The control of chlorophyll catabolism and the status of yellowing as a biomarker of leaf senescence. Plant Biology 10, 4–14.
| The control of chlorophyll catabolism and the status of yellowing as a biomarker of leaf senescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslajs78%3D&md5=f2e75f6a53dffec3ac8128a7f31e905eCAS | 18721307PubMed |
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety 60, 324–349.
| Salt tolerance and salinity effects on plants: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKlt7nN&md5=c6e53434303fd9123086083191a18670CAS | 15590011PubMed |
Plett DC, Moller IS (2010) Na+ transport in glycophytic plants: what we know and would like to know. Plant, Cell & Environment 33, 612–626.
| Na+ transport in glycophytic plants: what we know and would like to know.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2hu7w%3D&md5=b8f7ef5ebf4603dbe012fea2f42155deCAS | 19968828PubMed |
Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant, Cell & Environment 32, 237–249.
| Quantifying the three main components of salinity tolerance in cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVKlsL4%3D&md5=e3804088de47e2567ad7e0d60304ace8CAS | 19054352PubMed |
Shabala S (2009) Salinity and programmed cell death: unraveling mechanisms for ion specific signalling. Journal of Experimental Botany 60, 709–712.
| Salinity and programmed cell death: unraveling mechanisms for ion specific signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFSmsLg%3D&md5=51021609fecf6a11aa6c680995a6b95bCAS | 19269993PubMed |
Shabala S, Shabala L, Van Volkenburgh E (2003) Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Functional Plant Biology 30, 507–514.
| Effect of calcium on root development and root ion fluxes in salinised barley seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtFWgtL4%3D&md5=8b6f9c269daaaac49c0276315e5584a3CAS |
Shabala S, Shabala S, Cuin TA, Pang J, Percey W, Chen Z, Conn S, Eing C, Wegner LH (2010) Xylem ionic relations and salinity tolerance in barley. The Plant Journal 61, 839–853.
| Xylem ionic relations and salinity tolerance in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsFaktr0%3D&md5=e1046f15f5387404d89efaad2fc282d9CAS | 20015063PubMed |
Smethurst CF, Gill WM, Shabala S (2009) Using excised leaves to screen lucerne for salt tolerance. Plant Signaling & Behavior 4, 39–41.
| Using excised leaves to screen lucerne for salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsVyqtbw%3D&md5=dea4dab5132d09db705f01d89ddf5900CAS | 19704703PubMed |
Tester MA, Davenport RJ (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
| Na+ tolerance and Na+ transport in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVyisbk%3D&md5=1d347e97621c3429b50d3bd9471ffd5eCAS | 12646496PubMed |
Vera-Estrella R, Barkla BJ, Garcia-Ramirez L, Pantoja O (2005) Salt stress in Thellungiella halophila activates Na+ transport mechanisms required for salinity tolerance. Plant Physiology 139, 1507–1517.
| Salt stress in Thellungiella halophila activates Na+ transport mechanisms required for salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Ogu73F&md5=987aa9627a940b9c2ed1f2c53bf6ae7cCAS | 16244148PubMed |
Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal 45, 523–539.
| Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislWit7w%3D&md5=239a1ba3f45c98fd8e0b5b4e0179f368CAS | 16441347PubMed |
Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. The Plant Cell 14, S131–S151.
Widodo , Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. Journal of Experimental Botany 60, 4089–4103.
| Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WqtLnF&md5=30cd3fc9599100e202538d75a2c44addCAS |
Xie C, Zhang ZG, Zhang JS, He XJ, Cao WH, He SJ, Chen SY (2002) Spatial expression and characterization of a putative ethylene receptor protein NTHK1 in tobacco. Plant & Cell Physiology 43, 810–815.
| Spatial expression and characterization of a putative ethylene receptor protein NTHK1 in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsFOitr8%3D&md5=e508176b1e4df00761c8ddaed671798fCAS | 12154144PubMed |
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=09a21ec11cd9567e1458a41ad4d4558bCAS | 16280254PubMed |
Yang YX, Jia YH, Nie LL, Zhang Y, Chen SY, Wang JA, Liu ZQ (2009) Relationship between accumulation of Na+ in leaves and salt tolerance of different Populus genotypes. Plant Physiology Communications 45, 1070–1074.
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=552a62148f6ddf231be6ce9e7241b945CAS | 11479571PubMed |
Zhang JS, Xie C, Shen YG, Chen SY (2001) A two-component gene (NTHK1) encoding a putative ethylene-receptor homolog is both developmentally and stress-regulated in tobacco. Theoretical and Applied Genetics 102, 815–824.
| A two-component gene (NTHK1) encoding a putative ethylene-receptor homolog is both developmentally and stress-regulated in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1SktLk%3D&md5=7e544e103be75464aedf4b31b0a3f6a5CAS |
Zhang WH, Yu BJ, Chen Q, Liu YL (2004) Tonoplast H+-ATPase activity in barley roots is regulated by ATP and pyrophosphate contents under NaCl stress. Journal of Plant Physiology and Molecular Biology 30, 45–52.
Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Over-expression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. Journal of Experimental Botany 60, 3781–3796.
| Over-expression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2ks7zL&md5=b2b5f783fc5ad160a37691e65c12c91cCAS | 19602544PubMed |
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology 6, 441–445.
| Regulation of ion homeostasis under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVKhsbs%3D&md5=7e54c59bd255571504f5829ff758b75fCAS | 12972044PubMed |
