A calcium sensor-interacting protein kinase negatively regulates salt stress tolerance in rice (Oryza sativa)
Xiao-Lan Rao A , Xiu-Hong Zhang A , Rong-Jun Li A , Hai-Tao Shi A and Ying-Tang Lu A B
+ Author Affiliations
- Author Affiliations
A State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China.
B Corresponding author. Email: yingtlu@whu.edu.cn
Functional Plant Biology 38(6) 441-450 https://doi.org/10.1071/FP10205
Submitted: 25 October 2010 Accepted: 27 April 2011 Published: 3 June 2011
Abstract
Protein kinases are signal transduction factors that play a central role in acclimation. In this study, the function of a calcium sensor-interacting protein kinase, OsCIPK03, was characterised in the salt stress response of rice (Oryza sativa L.). Transgenic plants overexpressing OsCIPK03 exhibited an increased sensitivity to salt stress during both seed germination and seedling growth. By contrast, transgenic RNA interference lines that underexpressed OsCIPK03 were significantly more tolerant to NaCl stress than the wild-type. In response to salt stress, rice that underexpressed OsCIPK03 accumulated more proline than non-transformed plants. Furthermore, several stress-responsive genes were identified as being differentially expressed in the transgenic plants. Together, these results suggest that OsCIPK03 functions as a negative regulator of salt stress tolerance in rice.
Additional keywords: calcineurin B-like protein-interacting protein kinases (CIPKs), negative regulator, transgenic plants.
References
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=100b7d568c0a92daa4d1ac981ff7c856CAS | 10455050PubMed |
Armengaud P, Thiery L, Buhot N, Grenier-De March G, Savoure A (2004) Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiologia Plantarum 120, 442–450.
| Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisVKhs78%3D&md5=a1b08ee8bd479ce68c01936c4d9aea47CAS | 15032841PubMed |
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
| Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlsVGitLk%3D&md5=c827b48f99c0b89e93d36acb1c0f9680CAS |
Batistic O, Kudla J (2004) Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta 219, 915–924.
| Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotlKgtbw%3D&md5=840aac70d3755d181a811d8774b01269CAS | 15322881PubMed |
Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. The Plant Journal 52, 223–239.
| Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSis7nN&md5=f5082368b7ca868e380c4c10bcbaacbaCAS | 17922773PubMed |
DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. The Biochemical Journal 425, 27–40.
| Breaking the code: Ca2+ sensors in plant signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Sru7vM&md5=82c3f335d8afd7e7a12a0233ba0e1bccCAS |
Diédhiou CJ, Popova OV, Dietz KJ, Golldack D (2008) The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biology 8, 49
| The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice.Crossref | GoogleScholarGoogle Scholar | 18442365PubMed |
Fuchs I, Stolzle S, Ivashikina N, Hedrich R (2005) Rice K+ uptake channel OsAKT1 is sensitive to salt stress. Planta 221, 212–221.
| Rice K+ uptake channel OsAKT1 is sensitive to salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvVCmsrs%3D&md5=baa276528f69d4b41ce7910948d01209CAS | 15599592PubMed |
Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proceedings of the National Academy of Sciences of the United States of America 97, 3735–3740.
| The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitlajsrg%3D&md5=71eab71636ea88f7bb8843108d0e7b4aCAS | 10725350PubMed |
Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant, Cell & Environment 21, 535–553.
| Dissecting the roles of osmolyte accumulation during stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltl2hu7s%3D&md5=c2f11517bfc0a34c59bd80b0ab511120CAS |
Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. The Plant Journal 6, 271–282.
| Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtlGntLc%3D&md5=e6667dd733fa9f34d8cc5e481dd2018aCAS | 7920717PubMed |
Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu J-K, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiology 132, 666–680.
| The Arabidopsis CDPK-SnRK superfamily of protein kinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslertr8%3D&md5=99b4d360f8a6462660c03f89f8163404CAS | 12805596PubMed |
Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiology 77, 483–485.
| Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht12jtrc%3D&md5=3c10cd2a3e29b859d296d2af1d57f466CAS | 16664080PubMed |
Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. The Plant Cell 15, 411–423.
| CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlOmtbo%3D&md5=00937547a0b8464b3623d1b1bca18859CAS | 12566581PubMed |
Knight H (2000) Calcium signaling during abiotic stress in plants. International Review of Cytology 195, 269–324.
| Calcium signaling during abiotic stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVehu7o%3D&md5=41716f1ac83a596b7fa6ffb4b686fad7CAS | 10603578PubMed |
Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL–CIPK signaling networks. Plant Physiology 134, 43–58.
| Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL–CIPK signaling networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVagtbo%3D&md5=13582bfebf79157163699059967da02eCAS | 14730064PubMed |
Kurusu T, Hamada J, Hamada H, Hanamata S, Kuchitsu K (2010) Roles of calcineurin B-like protein-interacting protein kinases in innate immunity in rice. Plant Signaling & Behavior 5, 1045–1047.
| Roles of calcineurin B-like protein-interacting protein kinases in innate immunity in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs12kt74%3D&md5=db609a179ef8a467efea435b4b92bc1cCAS | 20724838PubMed |
Lee KW, Chen PW, Lu CA, Chen S, Ho TH, Yu SM (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Science Signaling 2, ra61
| Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding.Crossref | GoogleScholarGoogle Scholar | 19809091PubMed |
Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca(2)+ signaling pathway regulates a K(+) channel for low-K response in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 12625–12630.
| A Ca(2)+ signaling pathway regulates a K(+) channel for low-K response in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XoslSmtb4%3D&md5=b5180e118635afce960ee6ba5b16034aCAS | 16895985PubMed |
Liu J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiology 114, 591–596.
| Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktVSks78%3D&md5=7bf7bc1fb5b7a33f4482bf263075b606CAS | 9193091PubMed |
Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proceedings of the National Academy of Sciences of the United States of America 97, 3730–3734.
| The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitlajsrs%3D&md5=ffbb1e844c43b9ca6a50b6c3e2f18b7dCAS | 10725382PubMed |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=fb7f5980d7bf4d62f797a1988cd8f193CAS | 11846609PubMed |
Luan S (2009) The CBL–CIPK network in plant calcium signaling. Trends in Plant Science 14, 37–42.
| The CBL–CIPK network in plant calcium signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntVyhuw%3D%3D&md5=500334dafafc744f632e00b9324dec53CAS | 19054707PubMed |
Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. The Plant Cell 14, S389–S400.
Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. Journal of Experimental Botany 46, 1843–1852.
| Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsFeguw%3D%3D&md5=d0f53b7a4d7e2f702218a3bc143fd72cCAS |
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Archives of Biochemistry and Biophysics 444, 139–158.
| Cold, salinity and drought stresses: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Olt7fI&md5=00a4e74c12eca6b8fba2d63483176f36CAS | 16309626PubMed |
Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant & Cell Physiology 45, 490–495.
| Simple RNAi vectors for stable and transient suppression of gene function in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKhtbs%3D&md5=429d11e157b65bb0ae07e245099e3a96CAS | 15111724PubMed |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bioassays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=06c472aaff717f5157aa29da67ee5ad0CAS |
Niu X, Chen Q, Wang X (2008) OsITL1 gene encoding an inositol 1,3,4-trisphosphate 5/6-kinase is a negative regulator of osmotic stress signaling. Biotechnology Letters 30, 1687–1692.
| OsITL1 gene encoding an inositol 1,3,4-trisphosphate 5/6-kinase is a negative regulator of osmotic stress signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvVKls7k%3D&md5=35ed28fa80e22932f22e66ce4017a7e5CAS | 18421420PubMed |
Pandey GK, Grant JJ, Cheong YH, Kim BG, Li LG, Luan S (2008) Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination. Molecular Plant 1, 238–248.
| Calcineurin-B-like protein CBL9 interacts with target kinase CIPK3 in the regulation of ABA response in seed germination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslyks7w%3D&md5=57e00c7032865b16ef25b8a83805d4d1CAS | 19825536PubMed |
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 |
Piao HL, Xuan YH, Park SH, Je BI, Park SJ, Park SH, Kim CM, Huang J, Wang GK, Kim MJ, Kang SM, Lee IJ, Kwon TR, Kim YH, Yeo US, Yi G, Son D, Han CD (2010) OsCIPK31, a CBL-interacting protein kinase, is involved in germination and seedling growth under abiotic stress conditions in rice plants. Molecules and Cells 30, 19–27.
| OsCIPK31, a CBL-interacting protein kinase, is involved in germination and seedling growth under abiotic stress conditions in rice plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptFGmtbs%3D&md5=1a4a4f8814268847fbb5674347b83ae5CAS | 20652492PubMed |
Platten JD, Cotsaftis O, Berthomieu P, Bohnert H, Davenport RJ, Fairbairn DJ, Horie T, Leigh RA, Lin HX, Luan S, Mäser P, Pantoja O, Rodríguez-Navarro A, Schachtman DP, Schroeder JI, Sentenac H, Uozumi N, Véry AA, Zhu JK, Dennis ES, Tester M (2006) Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends in Plant Science 11, 372–374.
| Nomenclature for HKT transporters, key determinants of plant salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xns1Kjur8%3D&md5=223723805945f45f7c16d0bc9aa9b220CAS | 16809061PubMed |
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proceedings of the National Academy of Sciences of the United States of America 99, 8436–8441.
| Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVGntrg%3D&md5=85af3b1b2f362f82dc3015a617d35c67CAS | 12034882PubMed |
Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proceedings of the National Academy of Sciences of the United States of America 99, 9061–9066.
| Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltF2hu70%3D&md5=aabdc94b874dad91b7e7c12c750b80bfCAS | 12070350PubMed |
Rabbani MA, Maruyama K, Rabbani M, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiology 133, 1755–1767.
| Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFCr&md5=909cdf99eda6288d447d9f9391f82607CAS | 14645724PubMed |
Rus A, Yokoi S, Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proceedings of the National Academy of Sciences of the United States of America 98, 14150–14155.
| AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVyms7k%3D&md5=0b7a23116bca18f8795bfd33d6d16163CAS | 11698666PubMed |
Rus A, Lee BH, Munoz-Mayor A, Sharkhuu A, Miura K, Zhu JK, Bressan RA, Hasegawa PM (2004) AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiology 136, 2500–2511.
| AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOrur4%3D&md5=140d0ddda805a636749872de8d41f677CAS | 15347798PubMed |
Sakakibara Y, Kobayashi H, Kasamo K (1996) Isolation and characterization of cDNAs encoding vacuolar H(+)-pyrophosphatase isoforms from rice (Oryza sativa L.). Plant Molecular Biology 31, 1029–1038.
| Isolation and characterization of cDNAs encoding vacuolar H(+)-pyrophosphatase isoforms from rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtFGisrs%3D&md5=2d41e1616aa4166df33efc141e278001CAS | 8843945PubMed |
Shi H, Zhu JK (2002) Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Molecular Biology 50, 543–550.
| Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmt12rsbk%3D&md5=dbdd3290084c49ab26448c65763d274aCAS | 12369629PubMed |
Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. The Plant Cell 11, 2393–2405.
Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na(+)/H(+) antiporter SOS1 controls long-distance Na(+) transport in plants. The Plant Cell 14, 465–477.
| The putative plasma membrane Na(+)/H(+) antiporter SOS1 controls long-distance Na(+) transport in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisVKgur0%3D&md5=53bda737c6aeabf6cfe4b4626573b034CAS | 11884687PubMed |
Weinl S, Kudla J (2009) The CBL–CIPK Ca(2+)-decoding signaling network: function and perspectives. New Phytologist 184, 517–528.
| The CBL–CIPK Ca(2+)-decoding signaling network: function and perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVOgs7vE&md5=4e9cbc75952fa3bd2eeb3e450e22d205CAS | 19860013PubMed |
Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiology 144, 1416–1428.
| Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1OlsLw%3D&md5=653c031175ce696a4a7d37a6eacb3346CAS | 17535819PubMed |
Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125, 1347–1360.
| A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvVGrs7s%3D&md5=98a34e9ea71a96068e152e1083eda022CAS | 16814720PubMed |
Yang W, Kong Z, Omo-Ikerodah E, Xu W, Li Q, Xue Y (2008) Calcineurin B-like interacting protein kinase OsCIPK23 functions in pollination and drought stress responses in rice (Oryza sativa L.). Journal of Genetics and Genomics 35, 531–543.
| Calcineurin B-like interacting protein kinase OsCIPK23 functions in pollination and drought stress responses in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1aitbrJ&md5=6685844d8994991b9c7b19560602d29eCAS | 18804072PubMed |
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 |
Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis. Evidence for a critical role of potassium nutrition. The Plant Cell 10, 1181–1191.
