Skip to main content
Log in

Trans-acting factor designated OSBZ8 interacts with both typical abscisic acid responsive elements as well as abscisic acid responsive element-like sequences in the vegetative tissues of indica rice cultivars

  • Biotic and Abiotic Stress
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Specific cis-acting elements, identified in the stress-regulated promoters, can respond to the changes in the levels of abscisic acid. Most of our previous works were done with ACGT-containing typical abscisic acid responsive elements (ABREs) but not with non-ACGT, GC-rich sequences also present in such promoters. The current communication shows a comparative analysis performed on the binding of rice nuclear proteins, together with the purified transcription factor OSBZ8, to the cis-elements in the promoters of Rab16A (Motif I/Motif II), Osem (Motif A-1/Motif B) and Em (4X ABRE/2X ABRC). Our data show that the extent of binding of nuclear protein from salt-tolerant rice to both typical ABREs and non-ACGT, ABRE-like sequences such as Motif IIa, is much higher than that from salt-sensitive rice and occurs constitutively, i.e., even with the protein from unstressed plants. The complex formation is low and inducible only by salt in the salt-sensitive variety. While Motif I bind to a single 38 kDa protein, Motif IIa bind to two polypeptides of 38 and 29 kDa. We also show here that the activation and binding of OSBZ8 to the upstream regions of salt-inducible genes depends on its phosphorylated state. The novelty of our work is that it shows rice OSBZ8 as the prime factor interacting with both typical ABRE(s) and ABRE-like sequences. To our knowledge, this is also the first report for the detection and identification of Motif IIa (non-ACGT, coupling element-like)-binding factor(s) from rice and their expression pattern in different rice cultivars.

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

Abbreviations

ABA:

Abscisic acid

ABRE:

Abscisic acid responsive element

ABRC:

Abscisic acid responsive complex

CE:

Coupling element

DRE:

Dehydration responsive element

EMSA:

Electrophoretic mobility shift assay

Rab:

Responsive to abscisic acid

RT-PCR:

Reverse transcriptase-polymerase chain reaction

References

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Blum H, Beier H, Gross HJ (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gel. Electrophoresis 8:93–99

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Busk PK, Pages M (1998) Regulation of abscisic acid-induced transcription. Plant Mol Biol 37:425–435

    Article  PubMed  CAS  Google Scholar 

  • Casaretto JA, Ho TH (2005) Transcriptional regulation by abscisic acid in barley (Hordeum vulgare L.) seeds involves autoregulation of transcription factor HvABI5. Plant Mol Biol 57:21–34

    Article  PubMed  CAS  Google Scholar 

  • Chae MJ, Lee JS, Naam MH, Cho K, Hong JY, Yi SA, Suh SC, Yoon IS (2007) A rice dehydration-inducible SNF1-related protein kinase 2 phosphorylates an abscisic acid responsive element-binding factor and associates with ABA signaling. Plant Mol Biol 63(2):151–169

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single step method of RNA isolation by acid guanidium thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought, high salt and cold responsive gene expression. Plant J 33:751–763

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein RR, Rock CD (2002) Abscisic acid biosynthesis and response. The Arabidopsis book. In: Somerville CR, Meyerowitz EM (eds) American Society of Plant Biologists, pp 1–48

  • Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth and gene expression in Arabidopsis. Plant Cell 19(2):485–494

    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(6):1988–1993

    Article  PubMed  CAS  Google Scholar 

  • Furtado A, Henry RJ (2005) The wheat Em promoter drives reporter gene expression in embryo and aleurone tissues of transgenic barley and rice. Plant Biotechnol J 3(4):421–434

    Article  PubMed  CAS  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157

    Article  PubMed  CAS  Google Scholar 

  • Gupta S, Chattopadhyay MK, Chatterjee P, Ghosh B, Sengupta DN (1998) Expression of abscisic acid-responsive element-binding protein in salt-tolerant indica rice (Oryza sativa L. cv. Pokkali). Plant Mol Biol 37:629–637

    Article  PubMed  CAS  Google Scholar 

  • Hattori T, Terada T, Hamasuna S (1995) Regulation of Osem gene and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. Plant J 7(6):913–925

    Article  PubMed  CAS  Google Scholar 

  • Hobo T, Kowyama Y, Hattori T (1999a) 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 

  • Hobo T, Asada M, Kowyama Y, Hattori T (1999b) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19(6):679–689

    Article  PubMed  CAS  Google Scholar 

  • Ishige F, Takaichi M, Foster R, Chua N-H, Oeda K (1999) A G-box motif (GCCACGTGCC) tetramer confers high-level constitutive expression in dicot and monocot plants. Plant J 18(4):443–448

    Article  CAS  Google Scholar 

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

  • 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 

  • Klimczak IJ, Scindler U, Cashmore AR (1992) DNA binding activity of the Arabidopsis G-box binding factor GBF1 is stimulated by phosphorylation by casein kinase II from broccoli. Plant Cell 1:969–976

    Google Scholar 

  • Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44:939–949

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low temperature-responsive gene expression respectively in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed  CAS  Google Scholar 

  • Marcotte WR Jr, Russell SH, Quatrano RS (1989) Abscisic acid-responsive sequences from the Em gene of wheat. Plant Cell 1:969–976

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee K, Roy Choudhury A, Gupta B, Gupta S, Sengupta DN (2006) An ABRE-binding factor, OSBZ8, is highly expressed in salt tolerant cultivars than in salt sensitive cultivars of indica rice. BMC Plant Biol 6:18

    Article  PubMed  Google Scholar 

  • Mundy J, Chua N-H (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7:2275–2287

    Google Scholar 

  • Mundy J, Yamaguchi-Shinozaki K, Chua N-H (1990) Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc Natl Acad Sci USA 87:1406–1410

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa H, Ohmiya K, Hattori T (1996) A rice bZIP protein, designated OSBZ8, is rapidly induced by abscisic acid. Plant J 9(2):217–227

    Article  PubMed  CAS  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high salinity-stresses. Plant J 34(2):137–148

    Article  PubMed  CAS  Google Scholar 

  • Ono A, Izawa T, Chua N-H, Shimamoto K (1996) The rab16B promoter of rice contains two distinct abscisic acid-responsive elements. Plant Physiol 112:483–491

    Article  PubMed  CAS  Google Scholar 

  • Pla M, Vilardell J, Guiltinan M, Marcotte B, Niogret MF, Quatrano RS, Pages M (1993) The cis regulatory element CCACGTGG is involved in ABA and water stress responses of the maize gene rab28. Plant Mol Biol 21:259–266

    Article  PubMed  CAS  Google Scholar 

  • Ross C, Shen QJ (2006) Computational prediction and experimental verification of HVA1-like abscisic acid responsive promoters in rice (Oryza sativa). Plant Mol Biol 62:233–246

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, vol 1, 2, 3, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10(3):296–302

    Article  PubMed  CAS  Google Scholar 

  • Shen Q, Ho TH (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes, each containing a G-box and a novel cis-acting element. Plant Cell 7:295–307

    Article  PubMed  CAS  Google Scholar 

  • Shen Q, Scott JU, Ho TH (1993) Hormone response complex in a novel abscisic acid and cycloheximide-inducible barley gene. J Biol Chem 268(31):23652–23660

    PubMed  CAS  Google Scholar 

  • Shen Q, Zhang P, Ho TH (1996) Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 8:1107–1119

    Article  PubMed  CAS  Google Scholar 

  • Shen QJ, Casaretto JA, Zhang P, Ho TH (2004) Functional definition of ABA-response complexes: the promoter units necessary and sufficient for ABA induction of gene expression in barley (Hordeum vulgare L.). Plant Mol Biol 54:111–124

    Article  PubMed  CAS  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 

  • Skriver K, Olsen FL, Rogers JC, Mundy J (1991) Cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc Natl Acad Sci USA 88:7266–7270

    Article  PubMed  CAS  Google Scholar 

  • Straub PF, Shen Q, Ho TD (1994) Structure and promoter analysis of an ABA and stress-regulated barley gene, HVA1. Plant Mol Biol 26:617–630

    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(21):11632–11637

    Article  PubMed  CAS  Google Scholar 

  • Vinson CR, Hai T, Boyd SM (1993) Dimerization specificity of the leucine zipper-containing bZIP motif on DNA binding: prediction and rational design. Genes Dev 7:1047–1058

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic and cold-stress responsive promoters. Trends Plant Sci 10(2):88–94

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Mundy J, Chua N-H (1989) Four tightly linked rab genes are differentially expressed in rice. Plant Mol Biol 14:29–39

    Article  Google Scholar 

Download references

Acknowledgments

The Department of Biotechnology (DBT), Government of India, New Delhi (Grant No.BT/PR2965/AGR/02/155/04/2002), financially supported this work. ARC acknowledges DBT for providing the award of Senior Research Fellowship during the course of this work. The authors gratefully acknowledge the excellent technical assistance of Mr. Jadab Ghosh, who has made painstaking efforts and taken special care in designing all the figures and photographs included in this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dibyendu N. Sengupta.

Additional information

Communicated by A. Atanassov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

RoyChoudhury, A., Gupta, B. & Sengupta, D.N. Trans-acting factor designated OSBZ8 interacts with both typical abscisic acid responsive elements as well as abscisic acid responsive element-like sequences in the vegetative tissues of indica rice cultivars. Plant Cell Rep 27, 779–794 (2008). https://doi.org/10.1007/s00299-007-0498-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-007-0498-1

Keywords

Navigation