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Plant Molecular Biology

, Volume 67, Issue 6, pp 589–602 | Cite as

Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice

  • Qiuyun Wang
  • Yucheng Guan
  • Yaorong Wu
  • Honglin Chen
  • Fan ChenEmail author
  • Chengcai ChuEmail author
Article

Abstract

DREB transcription factors play key roles in plant stress signalling transduction pathway, they can specifically bind to DRE/CRT element (G/ACCGAC) and activate the expression of many stress inducible genes. Here, a novel rice DREB transcription factor, OsDREB1F, was cloned and characterised via subtractive suppression hybridisation (SSH) from upland rice. Expression analysis revealed that OsDREB1F gene was induced by salt, drought, cold stresses, and also ABA application, but not by pathogen, wound, and H2O2. Subcellular localization results indicated that OsDREB1F localizes in nucleus. Yeast activity assay demonstrated that OsDREB1F gene encodes a transcription activator, and can specifically bind to DRE/CRT but not to ABRE element. Transgenic plants harbouring OsDREB1F gene led to enhanced tolerance to salt, drought, and low temperature in both rice and Arabidopsis. The further characterisation of OsDREB1F-overexpressing Arabidopsis showed that, besides activating the expression of COR genes which contain DRE/CRT element in their upstream promoter regions, the expression of rd29B and RAB18 genes were also activated, suggested that OsDREB1F may also participate in ABA-dependent pathway.

Keywords

OsDREB1F Transcription activator Abiotic stress tolerance Rice 

Abbreviations

ABA

Abscisic acid

CaMV

Cauliflower mosaic virus

DRE

Dehydration responsive element

DREB

DRE binding protein

CRT

C-repeat

CBF

C-repeat binding factor

AP2

APETALA2

EREBP

Ethylene responsive element binding factor

TF

Transcription factor

COR

Cold regulated genes

GFP

Green fluorescent protein

Notes

Acknowledgements

Here we thank Prof. Weicai Yang at Institute of Genetics and Developmental Biology, the Chinese Academy of Sciences, for his generosity on use of his confocal microscope. This work was supported by grants from Chinese Academy of Sciences (KSCX2-YW-N-010) and Ministry of Science and Technology of China (2005CB120806) and also National Natural Sciences Foundation of China (30621001).

References

  1. Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645PubMedCrossRefGoogle Scholar
  2. Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713PubMedCrossRefGoogle Scholar
  3. Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52PubMedCrossRefGoogle Scholar
  4. Buttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc Natl Acad Sci USA 94:5961–5966PubMedCrossRefGoogle Scholar
  5. Chen M, Wang QY, Cheng XG, Xu ZS, Li LC, Ye XG, Xia LQ, Ma YZ (2007) GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem Biophys Res Commun 353:299–305PubMedCrossRefGoogle Scholar
  6. Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054PubMedCrossRefGoogle Scholar
  7. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451PubMedCrossRefGoogle Scholar
  8. Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129:1781–1787PubMedCrossRefGoogle Scholar
  9. Chuck G, Meeley RB, Hake S (1998) The control of maize spikelet meristem fate by the APETALA2-like gene indeterminate spikelet1. Genes Dev 12:1145–1154PubMedCrossRefGoogle Scholar
  10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
  11. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243–15248PubMedCrossRefGoogle Scholar
  12. 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 33:751–763PubMedCrossRefGoogle Scholar
  13. Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168PubMedCrossRefGoogle Scholar
  14. Feng JX, Liu D, Pan Y, Gong W, Ma LG, Luo JC, Deng XW, Zhu YX (2005) An annotation update via cDNA sequence analysis and comprehensive profiling of developmental, hormonal or environmental responsiveness of the Arabidopsis AP2/EREBP transcription factor gene family. Plant Mol Biol 59:853–868PubMedCrossRefGoogle Scholar
  15. Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054PubMedCrossRefGoogle Scholar
  16. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404PubMedCrossRefGoogle Scholar
  17. Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49:459–471PubMedCrossRefGoogle Scholar
  18. Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442PubMedCrossRefGoogle Scholar
  19. Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781PubMedCrossRefGoogle Scholar
  20. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471PubMedCrossRefGoogle Scholar
  21. Gu YQ, Wildermuth MC, Chakravarthy S, Loh YT, Yang C, He X, Han Y, Martin GB (2002) Tomato transcription factors pti4, pti5, and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 14:817–831PubMedCrossRefGoogle Scholar
  22. Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648PubMedCrossRefGoogle Scholar
  23. Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. J Biol Chem 273:26857–26861PubMedCrossRefGoogle Scholar
  24. Hong JP, Kim WT (2005) Isolation and functional characterization of the Ca-DREBLP1 gene encoding a dehydration-responsive element binding-factor-like protein 1 in hot pepper (Capsicum annuum L. cv. Pukang). Planta 220:875–888PubMedCrossRefGoogle Scholar
  25. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153PubMedCrossRefGoogle Scholar
  26. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106PubMedCrossRefGoogle Scholar
  27. Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225PubMedCrossRefGoogle Scholar
  28. Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci USA 102:3117–3122PubMedCrossRefGoogle Scholar
  29. Kagaya Y, Ohmiya K, Hattori T (1999) RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res 27:470–478PubMedCrossRefGoogle Scholar
  30. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291PubMedCrossRefGoogle Scholar
  31. Kim SY, Kim YC, Lee JH, Oh SK, Chung E, Lee S, Lee YH, Choi D, Park JM (2005) Identification of a CaRAV1 possessing an AP2/ERF and B3 DNA-binding domain from pepper leaves infected with Xanthomonas axonopodis pv. glycines 8ra by differential display. Biochim Biophys Acta 1729:141–146PubMedGoogle Scholar
  32. Kizis D, Pages M (2002) Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. Plant J 30:679–689PubMedCrossRefGoogle Scholar
  33. Kizis D, Lumbreras V, Pages M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189PubMedCrossRefGoogle Scholar
  34. Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153PubMedCrossRefGoogle Scholar
  35. Krizek BA, Prost V, Macias A (2000) AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. Plant Cell 12:1357–1366PubMedCrossRefGoogle Scholar
  36. 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 10:1391–1406PubMedCrossRefGoogle Scholar
  37. Liu XQ, Bai XQ, Qian Q, Wang XJ, Chen MS, Chu CC (2005) OsWRKY03, a rice transcriptional activator that functions in defense signaling pathway upstream of OsNPR1. Cell Res 15:593–603PubMedCrossRefGoogle Scholar
  38. Liu JG, Zhang Z, Qin QL, Peng RH, Xiong AS, Chen JM, Xu F, Zhu H, Yao QH (2007a) Isolated and characterization of a cDNA encoding ethylene-responsive element binding protein (EREBP)/AP2-type protein, RCBF2, in Oryza sativa L. Biotechnol Lett 29:165–173PubMedCrossRefGoogle Scholar
  39. Liu XQ, Bai XQ, Wang XJ, Chu CC (2007b) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164(8):969–979PubMedCrossRefGoogle Scholar
  40. Maes T, Van de Steene N, Zethof J, Karimi M, D’Hauw M, Mares G, Van Montagu M, Gerats T (2001) Petunia AP2-like genes and their role in flower and seed development. Plant Cell 13:229–244PubMedCrossRefGoogle Scholar
  41. Menke FL, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO J 18:4455–4463PubMedCrossRefGoogle Scholar
  42. Modrusan Z, Reiser L, Feldmann KA, Fischer RL, Haughn GW (1994) Homeotic transformation of ovules into carpel-like structures in Arabidopsis. Plant Cell 6:333–349PubMedCrossRefGoogle Scholar
  43. Moose SP, Sisco PH (1996) Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev 10:3018–3027PubMedCrossRefGoogle Scholar
  44. Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101:3985–3990PubMedCrossRefGoogle Scholar
  45. Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182PubMedCrossRefGoogle Scholar
  46. Ohto MA, Fischer RL, Goldberg RB, Nakamura K, Harada JJ (2005) Control of seed mass by APETALA2. Proc Natl Acad Sci USA 102:3123–3128PubMedCrossRefGoogle Scholar
  47. Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081PubMedCrossRefGoogle Scholar
  48. Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046PubMedCrossRefGoogle Scholar
  49. Qiao ZX, Huang B, Liu JY (2008) Molecular cloning and functional analysis of an ERF gene from cotton (Gossypium hirsutum). Biochim Biophys Acta 1779:122–127PubMedGoogle Scholar
  50. Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052PubMedCrossRefGoogle Scholar
  51. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646PubMedCrossRefGoogle Scholar
  52. Rushton PJ, Bokowiec MT, Han S, Zhang H, Brannock JF, Chen X, Laudeman TW, Timko MP (2008) Tobacco transcription factors: novel insights into transcriptional regulation in the Solanaceae. Plant Physiol. Published on March 12, 2008. doi: 10.1104/pp.107.114041
  53. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009PubMedCrossRefGoogle Scholar
  54. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309PubMedCrossRefGoogle Scholar
  55. Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular responses to drought and cold stress. Curr Opin Biotechnol 7:161–167PubMedCrossRefGoogle Scholar
  56. Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334PubMedCrossRefGoogle Scholar
  57. Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Commun 250:161–170PubMedCrossRefGoogle Scholar
  58. Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436PubMedCrossRefGoogle Scholar
  59. Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen TH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551PubMedCrossRefGoogle Scholar
  60. Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12:3703–3714PubMedCrossRefGoogle Scholar
  61. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040PubMedCrossRefGoogle Scholar
  62. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599PubMedCrossRefGoogle Scholar
  63. Urao T, Yamaguchi-Shinozaki K, Rao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539PubMedCrossRefGoogle Scholar
  64. van der Fits L, Memelink J (2001) The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 25:43–53PubMedCrossRefGoogle Scholar
  65. van der Graaff E, Dulk-Ras AD, Hooykaas PJ, Keller B (2000) Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana. Development 127:4971–4980PubMedGoogle Scholar
  66. Weigel D (1995) The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell 7:388–389PubMedCrossRefGoogle Scholar
  67. Wilson K, Long D, Swinburne J, Coupland G (1996) A dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8:659–671PubMedCrossRefGoogle Scholar
  68. Wu YR, Wang QY, Ma YM, Chu CC (2005) Isolation and expression analysis of salt up-regulated ESTs in upland rice using PCR-based subtractive suppression hybridization method. Plant Sci 168:847–853CrossRefGoogle Scholar
  69. Xiong Y, Fei SZ (2006) Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.). Planta 224:878–888PubMedCrossRefGoogle Scholar
  70. 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-salt stress. Plant Cell 6:251–264PubMedCrossRefGoogle Scholar
  71. Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94PubMedCrossRefGoogle Scholar
  72. Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Tomo Y, Hayami N, Terada T, Shirouzu M, Osanai T, Tanaka A, Seki M, Shinozaki K, Yokoyama S (2004) Solution structure of the B3 DNA binding domain of the Arabidopsis cold-responsive transcription factor RAV1. Plant Cell 16:3448–3459PubMedCrossRefGoogle Scholar
  73. Zarka DG, Vogel JT, Cook D, Thomashow MF (2003) Cold induction of Arabidopsis CBF genes involves multiple ICE (inducer of CBF expression) promoter elements and a cold-regulatory circuit that is desensitized by low temperature. Plant Physiol 133:910–918PubMedCrossRefGoogle Scholar
  74. Zhou J, Tang X, Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16:3207–3218PubMedCrossRefGoogle Scholar
  75. Zhu QH, Hoque MS, Dennis ES, Upadhyaya NM (2003) Ds tagging of BRANCHED FLORETLESS 1 (BFL1) that mediates the transition from spikelet to floret meristem in rice (Oryza sativa L). BMC Plant Biol 3:6PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.State Key Laboratory of Plant Genomics and National Centre for Plant Gene Research (Beijing), Institute of Genetics and Developmental BiologyChinese Academy of Sciences (CAS)BeijingChina
  2. 2.Graduate University of the CAS BeijingChina
  3. 3.Laboratory of Molecular and Developmental Biology, Institute of Genetics and Developmental BiologyCASBeijingChina

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