Skip to main content

Advertisement

Log in

The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Abscisic acid (ABA)-responsive element binding proteins (AREBs) are basic domain/leucine zipper transcription factors that bind to the ABA-responsive element (ABRE) in the promoter regions of ABA-inducible genes in plants. A novel bZIP transcription factor gene, GmbZIP1, encoding 438 amino acids with a conserved bZIP domain composed of 60 amino acids was isolated from salt-tolerant soybean cv. Tiefeng 8. Southern blotting showed that only one copy was present in the soybean genome. Phylogenetic analyses showed that GmbZIP1 belonged to the AREB subfamily of the bZIP family and was most closely related to AtABF2 and OsTRAB1. The expression of GmbZIP1 was highly induced by ABA, drought, high salt and low temperature; and GmbZIP1 was expressed in soybean roots, stems and leaves under different stress conditions. GmbZIP1 was localized inside the nuclei of transformed onion epidermal cells. Overexpression of GmbZIP1 enhanced the responses of transgenic plants to ABA and triggered stomatal closure under stresses, potentially leading to improved tolerances to several abiotic stresses such as high salt, low temperature and drought in transgenic plants. Furthermore, overexpression of GmbZIP1 affected the expression of some ABA or stress-related genes involved in regulating stomatal closure in Arabidopsis under ABA, drought and high salt stress conditions. A few AREB elements were detected in the promoter region of those ABA or stress-related genes, suggesting that GmbZIP1 regulates the ABA response or stomatal closure mediated by those downstream genes in transgenic Arabidopsis. Moreover, GmbZIP1 was used to improve the drought tolerance trait of Chinese wheat varieties BS93. Functional analysis showed that overexpression of GmbZIP1 enhanced the drought tolerance of transgenic wheat, and transcripts of GmbZIP1 were detected in transgenic wheat using RT-PCR. In addition, GmbZIP1 overexpression did not result in growth retardation in all transgenic plants, suggesting that GmbZIP1 may be a valuable genetic resource for engineering stress tolerance of crops.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Anderson SJ, Abraham KM, Nakayama T, Singer A, Perlmutter RM (1992) Inhibition of T-cell receptor beta-chain gene rearrangement by overexpression of the non-receptor protein tyrosine kinase p56 l ck. EMBO J 11:4877–4886

    PubMed  CAS  Google Scholar 

  • Bechtold N, Pelletier G (1998) In planta Agrobacterium mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266

    PubMed  CAS  Google Scholar 

  • Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14:1391–1403

    Article  PubMed  CAS  Google Scholar 

  • Casaretto J, Ho T-HD (2003) The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15:271–284

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Gong Z, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50:1187–1195

    Article  PubMed  CAS  Google Scholar 

  • Choi H, Hong J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 21:1723–1730

    Article  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LP, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    Article  PubMed  CAS  Google Scholar 

  • Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez Mohammad M, Seki M, Keiichiro H, Masaru OT, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488

    Article  PubMed  CAS  Google Scholar 

  • Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993

    Article  PubMed  CAS  Google Scholar 

  • Guiltinan MJ, Marcotte WR Jr, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267–271

    Article  PubMed  CAS  Google Scholar 

  • Hattori T, Totsuka M, Hobo T, Kagaya Y, Yamamoto-Toyoda A (2002) Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant Cell Physiol 43:136–140

    Article  PubMed  CAS  Google Scholar 

  • Hobo T, Asada M, Kowyama Y, Hattori T (1999a) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19:679–689

    Article  PubMed  CAS  Google Scholar 

  • Hobo T, Kowyama Y, Hattori T (1999b) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid induced transcription. Proc Natl Acad Sci USA 96:15348–15353

    Article  PubMed  CAS  Google Scholar 

  • Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya TsaiYC, Chan MT (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231(6):1459–1473

    Article  PubMed  CAS  Google Scholar 

  • Ito T, Shinozaki K (2002) The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol 43:1285–1292

    Article  PubMed  CAS  Google Scholar 

  • Iwata Y, Fedoroff NV, Koizumi N (2008) Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20:3107–3121

    Article  PubMed  CAS  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  PubMed  CAS  Google Scholar 

  • Jin XF, Xiong AS, Peng RH, Liu JG, Gao F, Chen JM, Yao QH (2010) OsAREB1, an ABRE-binding protein responding to ABA and glucose, has multiple functions in Arabidopsis. Biochem Mol Biol Rep 43(1):34–39

    CAS  Google Scholar 

  • Johnson RR, Wagner RL, Verhey SD, Walker-Simmons MK (2002) The abscisic acid-responsive kinase PKABA1 interacts with a seed-specific abscisic acid response element binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiol 130:837–846

    Article  PubMed  Google Scholar 

  • Kagaya Y, Hobo T, Murata M, Ban A, Hattori T (2002) Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14:3177–3189

    Article  PubMed  CAS  Google Scholar 

  • Kang J, Choi H, Im M, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357

    Article  PubMed  CAS  Google Scholar 

  • Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45(3):346–350

    Article  PubMed  CAS  Google Scholar 

  • Kim SY, Chung HJ, Thomas TL (1997) Isolation of a novel class of bZIP transcription factors that interact with ABA responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant J 11:1237–1251

    Article  PubMed  CAS  Google Scholar 

  • Kim SY, Ma J, Perret P, Li Z, Thomas TL (2002) Arabidopsis ABI5 subfamily members have distinct DNA-binding and transcriptional activities. Plant Physiol 130:688–697

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Kang JY, Cho DI, Park JH, Kim SY (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40:75–87

    Article  PubMed  CAS  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222

    Article  PubMed  CAS  Google Scholar 

  • Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: Features of a calcium-modulated protein phosphatase. Science 264:1448–1452

    Article  PubMed  CAS  Google Scholar 

  • Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008a) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240

    Article  PubMed  CAS  Google Scholar 

  • Liao Y, Zhang JS, Chen SY, Zhang WK (2008b) Role of soybean GmbZIP132 under abscisic acid and salt stresses. J Integr Plant Biol 50:221–230

    Article  PubMed  CAS  Google Scholar 

  • Lu GJ, ChX Gao, Zheng XN, Han B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229:605–615

    Article  PubMed  CAS  Google Scholar 

  • 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 Physiol 49(8):1150–1164

    Article  PubMed  CAS  Google Scholar 

  • Ma S, Quist TM, Ulanov A, Joly R, Bohnert HJ (2004) Loss of TIP1; 1 aquaporin in Arabidopsis leads to cell and plant death. Plant J 40:845–859

    Article  PubMed  CAS  Google Scholar 

  • Menkens AE, Schindler U, Cashmore AR (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochem Sci 20:506–512

    Article  PubMed  CAS  Google Scholar 

  • Meyer K, Leube MP, Grill E (1994) A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264:1452–1455

    Article  PubMed  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acid Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  • Osakabe Y, Maruyama K, Seki M, Satou M, Shinozaki K, Yamaguchi-Shinozaki K (2005) Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 17:1105–1119

    Article  PubMed  CAS  Google Scholar 

  • Pei ZM, Ghassemian M, Kwak CM, McCourt P, Schroeder JI (1998) Role of farnesyl transferase in ABA regulation of guard cell anion channels and plant water loss. Science 282:287–290

    Article  PubMed  CAS  Google Scholar 

  • Pilot G, Lacombe B, Gaymard F, Cherel I, Boucherez J, Thibaud JB, Sentenac H (2001) Guard cell inward K+ channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2. J Biol Chem 276:3215–3221

    Article  PubMed  CAS  Google Scholar 

  • Sanford JC, Smith FD, Russell JA (1993) Optimizing the biolistic process for different biological applications. Methods Enzymol 217:483–509

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410:327–330

    Article  PubMed  CAS  Google Scholar 

  • Schütze K, Harter K, Chaban C (2008) Post-translational regulation of plant bZIP factors. Trends Plant Sci 13:247–255

    Article  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signalling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

  • Suzuki M, Ketterling MG, Li QB, McCarty DR (2003) Viviparous1 alters global gene expression patterns through regulation of abscisic acid signaling. Plant Physiol 132:1664–1677

    Article  PubMed  CAS  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    Article  PubMed  CAS  Google Scholar 

  • Wang P, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178:703–718

    Article  PubMed  CAS  Google Scholar 

  • Weltmeier F, Rahmani F, Ehlert A, Dietrich K, Wang X et al (2009) Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development. Plant Mol Biol 69:107–119

    Article  PubMed  CAS  Google Scholar 

  • Xiang Y, Tang N, Du H, Ye HY, Xiong LZH (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker K, Zhu JK (2002) Cell signaling during cold, drought and salt stress. Plant Cell 14(suppl):165–183

    Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salinity stress. Plant Cell 6:251–264

    Article  PubMed  CAS  Google Scholar 

  • Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473–1483

    Article  PubMed  CAS  Google Scholar 

  • Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61(4):672–685

    Article  PubMed  CAS  Google Scholar 

  • Zeevaart JAD, Creelman RA (1988) Metabolism and physiology of abscisic acid. Ann Rev Plant Physiol Plant Mol Biol 39:439–473

    Article  CAS  Google Scholar 

  • Zheng HJ, He SJ (1994) Some improvements of the biolistic transformation system for Oryza sativa L. Chinese Biotechnol 12:111–115

    Google Scholar 

Download references

Acknowledgments

We are thankful to the reviewers for their comments and suggestions. We are also grateful to Dr. Robert McIntosh (University of Sydney), Dr. Mao Long (Key Laboratory of Crop Genetics and Breeding, Ministry of Agriculture in Institute of Crop Science, CAAS) and International Science Editing Ltd for modifying this manuscript. The work was funded in part by the National Key Project for Research on Transgenic Biology (2008ZX08002-002), the National 863 High-tech Project (2008AA10Z124), the National Natural Science Foundation of China (30700504 and 30700508), the Beijing Nova Program (2008B035), Natural Science Foundation of Beijing (5102016) and the Young Science Foundation of Beijing Academy of Agricultural and Forestry Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to You-Zhi Ma.

Additional information

The authors Shi-Qing Gao and Ming Chen contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gao, SQ., Chen, M., Xu, ZS. et al. The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol Biol 75, 537–553 (2011). https://doi.org/10.1007/s11103-011-9738-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-011-9738-4

Keywords

Navigation