The chimeric repressor for the GATA4 transcription factor improves tolerance to nitrogen deficiency in Arabidopsis
Nitrogen limits crop yield, but application of nitrogen fertilizer can cause environmental problems and much fertilizer is lost without being absorbed by plants. Increasing nitrogen use efficiency in plants may help overcome these problems and is, therefore, an important and active subject of agricu...
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| Published in | Plant Biotechnology Vol. 34; no. 3; pp. 151 - 158 |
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| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Japan
Japanese Society for Plant Cell and Molecular Biology
2017
Japan Science and Technology Agency |
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| Online Access | Get full text |
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| Abstract | Nitrogen limits crop yield, but application of nitrogen fertilizer can cause environmental problems and much fertilizer is lost without being absorbed by plants. Increasing nitrogen use efficiency in plants may help overcome these problems and is, therefore, an important and active subject of agricultural research. Here, we report that the expression of the chimeric repressor for the GATA4 transcription factor (35S:GATA4-SRDX) improved tolerance to nitrogen deficiency in Arabidopsis thaliana. 35S:GATA4-SRDX seedlings were significantly larger than wild type under nitrogen-sufficient and -deficient conditions (10 and 0.5 mM NH4NO3, respectively). 35S:GATA4-SRDX plants exhibited shorter primary roots, fewer lateral roots, and higher root hair density compared with wild type. The expression levels of NITRATE TRANSPORTER 2.1, ASPARAGINE SYNTHETASE and NITRATE REDUCTASE 1 were significantly higher in roots of 35S:GATA4-SRDX plants than in wild type under nitrogen-sufficient conditions. Under nitrogen-deficient conditions, the expression of genes for cytosolic glutamine synthetases was upregulated in shoots of 35S:GATA4-SRDX plants compared with wild type. This upregulation of nitrogen transporter and nitrogen assimilation-related genes might confer tolerance to nitrogen deficiency in 35S:GATA4-SRDX plants. |
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| AbstractList | Nitrogen limits crop yield, but application of nitrogen fertilizer can cause environmental problems and much fertilizer is lost without being absorbed by plants. Increasing nitrogen use efficiency in plants may help overcome these problems and is, therefore, an important and active subject of agricultural research. Here, we report that the expression of the chimeric repressor for the GATA4 transcription factor (35S:GATA4-SRDX) improved tolerance to nitrogen deficiency in Arabidopsis thaliana. 35S:GATA4-SRDX seedlings were significantly larger than wild type under nitrogen-sufficient and -deficient conditions (10 and 0.5 mM NH4NO3, respectively). 35S:GATA4-SRDX plants exhibited shorter primary roots, fewer lateral roots, and higher root hair density compared with wild type. The expression levels of NITRATE TRANSPORTER 2.1, ASPARAGINE SYNTHETASE and NITRATE REDUCTASE 1 were significantly higher in roots of 35S:GATA4-SRDX plants than in wild type under nitrogen-sufficient conditions. Under nitrogen-deficient conditions, the expression of genes for cytosolic glutamine synthetases was upregulated in shoots of 35S:GATA4-SRDX plants compared with wild type. This upregulation of nitrogen transporter and nitrogen assimilation-related genes might confer tolerance to nitrogen deficiency in 35S:GATA4-SRDX plants.Nitrogen limits crop yield, but application of nitrogen fertilizer can cause environmental problems and much fertilizer is lost without being absorbed by plants. Increasing nitrogen use efficiency in plants may help overcome these problems and is, therefore, an important and active subject of agricultural research. Here, we report that the expression of the chimeric repressor for the GATA4 transcription factor (35S:GATA4-SRDX) improved tolerance to nitrogen deficiency in Arabidopsis thaliana. 35S:GATA4-SRDX seedlings were significantly larger than wild type under nitrogen-sufficient and -deficient conditions (10 and 0.5 mM NH4NO3, respectively). 35S:GATA4-SRDX plants exhibited shorter primary roots, fewer lateral roots, and higher root hair density compared with wild type. The expression levels of NITRATE TRANSPORTER 2.1, ASPARAGINE SYNTHETASE and NITRATE REDUCTASE 1 were significantly higher in roots of 35S:GATA4-SRDX plants than in wild type under nitrogen-sufficient conditions. Under nitrogen-deficient conditions, the expression of genes for cytosolic glutamine synthetases was upregulated in shoots of 35S:GATA4-SRDX plants compared with wild type. This upregulation of nitrogen transporter and nitrogen assimilation-related genes might confer tolerance to nitrogen deficiency in 35S:GATA4-SRDX plants. Nitrogen limits crop yield, but application of nitrogen fertilizer can cause environmental problems and much fertilizer is lost without being absorbed by plants. Increasing nitrogen use efficiency in plants may help overcome these problems and is, therefore, an important and active subject of agricultural research. Here, we report that the expression of the chimeric repressor for the GATA4 transcription factor (35S:GATA4-SRDX) improved tolerance to nitrogen deficiency in Arabidopsis thaliana. 35S:GATA4-SRDX seedlings were significantly larger than wild type under nitrogen-sufficient and -deficient conditions (10 and 0.5 mM NH4NO3, respectively). 35S:GATA4-SRDX plants exhibited shorter primary roots, fewer lateral roots, and higher root hair density compared with wild type. The expression levels of NITRATE TRANSPORTER 2.1, ASPARAGINE SYNTHETASE and NITRATE REDUCTASE 1 were significantly higher in roots of 35S:GATA4-SRDX plants than in wild type under nitrogen-sufficient conditions. Under nitrogen-deficient conditions, the expression of genes for cytosolic glutamine synthetases was upregulated in shoots of 35S:GATA4-SRDX plants compared with wild type. This upregulation of nitrogen transporter and nitrogen assimilation-related genes might confer tolerance to nitrogen deficiency in 35S:GATA4-SRDX plants. Nitrogen limits crop yield, but application of nitrogen fertilizer can cause environmental problems and much fertilizer is lost without being absorbed by plants. Increasing nitrogen use efficiency in plants may help overcome these problems and is, therefore, an important and active subject of agricultural research. Here, we report that the expression of the chimeric repressor for the GATA4 transcription factor ( 35S:GATA4-SRDX ) improved tolerance to nitrogen deficiency in Arabidopsis thaliana . 35S:GATA4-SRDX seedlings were significantly larger than wild type under nitrogen-sufficient and -deficient conditions (10 and 0.5 mM NH 4 NO 3 , respectively). 35S:GATA4-SRDX plants exhibited shorter primary roots, fewer lateral roots, and higher root hair density compared with wild type. The expression levels of NITRATE TRANSPORTER 2.1 , ASPARAGINE SYNTHETASE and NITRATE REDUCTASE 1 were significantly higher in roots of 35S:GATA4-SRDX plants than in wild type under nitrogen-sufficient conditions. Under nitrogen-deficient conditions, the expression of genes for cytosolic glutamine synthetases was upregulated in shoots of 35S:GATA4-SRDX plants compared with wild type. This upregulation of nitrogen transporter and nitrogen assimilation-related genes might confer tolerance to nitrogen deficiency in 35S:GATA4-SRDX plants. Nitrogen limits crop yield, but application of nitrogen fertilizer can cause environmental problems and much fertilizer is lost without being absorbed by plants. Increasing nitrogen use efficiency in plants may help overcome these problems and is, therefore, an important and active subject of agricultural research. Here, we report that the expression of the chimeric repressor for the GATA4 transcription factor ( ) improved tolerance to nitrogen deficiency in . seedlings were significantly larger than wild type under nitrogen-sufficient and -deficient conditions (10 and 0.5 mM NH NO , respectively). plants exhibited shorter primary roots, fewer lateral roots, and higher root hair density compared with wild type. The expression levels of , and were significantly higher in roots of plants than in wild type under nitrogen-sufficient conditions. Under nitrogen-deficient conditions, the expression of genes for cytosolic glutamine synthetases was upregulated in shoots of plants compared with wild type. This upregulation of nitrogen transporter and nitrogen assimilation-related genes might confer tolerance to nitrogen deficiency in plants. |
| Author | Ikeda, Miho Kojima, Soichi Chung, KwiMi Ohme-Takagi, Masaru Yeh, Chuan-Ming Mitsuda, Nobutaka Sakamoto, Shingo Shin, Ji Min |
| Author_xml | – sequence: 1 fullname: Shin, Ji Min organization: Graduate School of Science and Engineering, Saitama University – sequence: 2 fullname: Chung, KwiMi organization: Bioproduction Institute, Institute Advanced Industrial Science and Technology (AIST) – sequence: 3 fullname: Sakamoto, Shingo organization: Bioproduction Institute, Institute Advanced Industrial Science and Technology (AIST) – sequence: 4 fullname: Kojima, Soichi organization: Graduate School of Agricultural Science, Tohoku University – sequence: 5 fullname: Yeh, Chuan-Ming organization: Graduate School of Science and Engineering, Saitama University – sequence: 6 fullname: Ikeda, Miho organization: Graduate School of Science and Engineering, Saitama University – sequence: 7 fullname: Mitsuda, Nobutaka organization: Graduate School of Science and Engineering, Saitama University – sequence: 8 fullname: Ohme-Takagi, Masaru organization: Graduate School of Science and Engineering, Saitama University |
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| Copyright | 2017 by Japanese Society for Plant Cell and Molecular Biology Copyright Japan Science and Technology Agency 2017 2017 The Japanese Society for Plant Cell and Molecular Biology 2017 The Japanese Society for Plant Cell and Molecular Biology |
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| Keywords | transcription factor chimeric repressor nitrogen use efficiency Arabidopsis tolerance |
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| References | Giehl RFH, von Wirén N (2014) Root nutrient foraging. Plant Physiol 166: 509-517 Krapp A (2015) Plant nitrogen assimilation and its regulation: A complex puzzle with missing pieces. Curr Opin Plant Biol 25: 115-122 Orsel M, Krapp A, Daniel-Vedele F (2002) Analysis of the NRT2 nitrate transporter family in Arabidopsis: Structure and gene expression. Plant Physiol 129: 886-896 Manfield IW, Devlin PF, Jen CH, Westhead DR, Gilmartin PM (2006) Conservation, convergence, and divergence of light-responsive, circadian-regulated, and tissue-specific expression patterns during evolution of the Arabidopsis GATA gene family. Plant Physiol 143: 941-958 Vidal EA, Gutiérrez RA (2008) A system view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr Opin Plant Biol 11: 521-529 Carvalho HG, Lopes-Cardoso IA, Lima LG, Melo PM, Cullimore JV (2003) Nodule-specific modulation of glutamine synthetase in transgenic Medicago truncatula leads to inverse alterations in asparagine synthetase expression. Plant Physiol 133: 243-252 Engineer CB, Kranz RG (2007) Reciprocal leaf and root expression of AtAmt1.1 and root architectural changes in response to nitrogen starvation. Plant Physiol 143: 236-250 Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet 239: 289-297 Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407-409 Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63: 153-182 Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51: 227-237 Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11: 865-874 Wang R, Liu D, Crawford N (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci USA 95: 15134-15139 Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof transcription factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA 101: 7833-7838 Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochim Biophys Acta 1465: 219-235 Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wirén N (1999) Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11: 937-948 Marschner H (1995) Mineral Nutrition of Higher Plants, 2nd ed. Academic Press, London Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21: 3567-3584 Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, et al. (2000) Arabidopsis transcription factors: Genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110 Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Denneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806 Fuentes S, Allen D, Ortiz-Lopez A, Hernández G (2001) Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J Exp Bot 52: 1071-1081 Diaz C, Lemaître T, Christ C, Azzopardi M, Kato Y, Sato F, Morot-Gaudry JF, Dily FL, Masclaux-Daubresse C (2008) Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol 147: 1437-1449 Crawford NM, Forde BG (2002) Molecular and developmental biology in inorganic nitrogen nutrition. Arabidopsis Book 1: e0011 Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9: 597-605 Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoiki N, Ohsugi R (2011) Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biol J 9: 826-837 Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163: 161-179 Gilroy S, Jones DL (2000) Through form to function: Root hair development and nutrient uptake. Trends Plant Sci 5: 56-60 Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: Challenges for sustainable and productive agriculture. Ann Bot (Lond) 105: 1141-1157 Konishi M, Yanagisawa S (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat Commun 4: 1617 Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136: 2512-2522 Schultz ER, Zupanska AK, Sng SJ, Paul AL, Rerl RJ (2017) Skewing in Arabidopsis roots involves disparate environmental signaling pathways. BMC Plant Biol 17: 31 Orkin SH (1992) GATA-binding transcription factors in hematopoietic cells. Blood 80: 575-581 Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385: 59-61 Miflin RD, Lea PJ (1976) The pathway of nitrogen assimilation in plants. Phytochemistry 15: 873-885 Stitt M, Műller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible WR, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53: 959-970 Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34: 733-739 22 23 24 25 26 27 28 29 30 31 10 32 11 33 12 34 13 35 14 36 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
| References_xml | – reference: Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet 239: 289-297 – reference: Vidal EA, Gutiérrez RA (2008) A system view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr Opin Plant Biol 11: 521-529 – reference: Carvalho HG, Lopes-Cardoso IA, Lima LG, Melo PM, Cullimore JV (2003) Nodule-specific modulation of glutamine synthetase in transgenic Medicago truncatula leads to inverse alterations in asparagine synthetase expression. Plant Physiol 133: 243-252 – reference: Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoiki N, Ohsugi R (2011) Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biol J 9: 826-837 – reference: Crawford NM, Forde BG (2002) Molecular and developmental biology in inorganic nitrogen nutrition. Arabidopsis Book 1: e0011 – reference: Fuentes S, Allen D, Ortiz-Lopez A, Hernández G (2001) Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J Exp Bot 52: 1071-1081 – reference: Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407-409 – reference: Schultz ER, Zupanska AK, Sng SJ, Paul AL, Rerl RJ (2017) Skewing in Arabidopsis roots involves disparate environmental signaling pathways. BMC Plant Biol 17: 31 – reference: Diaz C, Lemaître T, Christ C, Azzopardi M, Kato Y, Sato F, Morot-Gaudry JF, Dily FL, Masclaux-Daubresse C (2008) Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol 147: 1437-1449 – reference: Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9: 597-605 – reference: Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11: 865-874 – reference: Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63: 153-182 – reference: Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Denneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806 – reference: Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, et al. (2000) Arabidopsis transcription factors: Genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110 – reference: Stitt M, Műller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible WR, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53: 959-970 – reference: Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136: 2512-2522 – reference: Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21: 3567-3584 – reference: Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wirén N (1999) Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11: 937-948 – reference: Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163: 161-179 – reference: Orsel M, Krapp A, Daniel-Vedele F (2002) Analysis of the NRT2 nitrate transporter family in Arabidopsis: Structure and gene expression. Plant Physiol 129: 886-896 – reference: Giehl RFH, von Wirén N (2014) Root nutrient foraging. Plant Physiol 166: 509-517 – reference: Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: Challenges for sustainable and productive agriculture. Ann Bot (Lond) 105: 1141-1157 – reference: Miflin RD, Lea PJ (1976) The pathway of nitrogen assimilation in plants. Phytochemistry 15: 873-885 – reference: Krapp A (2015) Plant nitrogen assimilation and its regulation: A complex puzzle with missing pieces. Curr Opin Plant Biol 25: 115-122 – reference: Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51: 227-237 – reference: Gilroy S, Jones DL (2000) Through form to function: Root hair development and nutrient uptake. Trends Plant Sci 5: 56-60 – reference: Konishi M, Yanagisawa S (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat Commun 4: 1617 – reference: Manfield IW, Devlin PF, Jen CH, Westhead DR, Gilmartin PM (2006) Conservation, convergence, and divergence of light-responsive, circadian-regulated, and tissue-specific expression patterns during evolution of the Arabidopsis GATA gene family. Plant Physiol 143: 941-958 – reference: Engineer CB, Kranz RG (2007) Reciprocal leaf and root expression of AtAmt1.1 and root architectural changes in response to nitrogen starvation. Plant Physiol 143: 236-250 – reference: Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof transcription factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA 101: 7833-7838 – reference: Wang R, Liu D, Crawford N (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci USA 95: 15134-15139 – reference: Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochim Biophys Acta 1465: 219-235 – reference: Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34: 733-739 – reference: Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385: 59-61 – reference: Marschner H (1995) Mineral Nutrition of Higher Plants, 2nd ed. Academic Press, London – reference: Orkin SH (1992) GATA-binding transcription factors in hematopoietic cells. 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| Snippet | Nitrogen limits crop yield, but application of nitrogen fertilizer can cause environmental problems and much fertilizer is lost without being absorbed by... |
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| SubjectTerms | Agricultural research Ammonium nitrate Arabidopsis Asparagine Aspartate-ammonia ligase chimeric repressor Crop yield Fertilizers Gene expression Genes Glutamine Nitrate reductase Nitrogen nitrogen use efficiency Roots Seedlings Shoots Short Communication tolerance transcription factor Transcription factors |
| Title | The chimeric repressor for the GATA4 transcription factor improves tolerance to nitrogen deficiency in Arabidopsis |
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