, Volume 231, Issue 6, pp 1459–1473

A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response

  • Tsai-Hung Hsieh
  • Chia-Wen Li
  • Ruey-Chih Su
  • Chiu-Ping Cheng
  • Sanjaya
  • Yi-Chien Tsai
  • Ming-Tsair Chan
Original Article


Abiotic stresses such as cold, water deficit, and salt stresses severely reduce crop productivity. Tomato (Solanum lycopersicum) is an important economic crop; however, not much is known about its stress responses. To gain insight into stress-responsive gene regulation in tomato plants, we identified transcription factors from a tomato cDNA microarray. An ABA-responsive element binding protein (AREB) was identified and named SlAREB. In tomato protoplasts, SlAREB transiently transactivated luciferase reporter gene expression driven by AtRD29A (responsive to dehydration) and SlLAP (leucine aminopeptidase) promoters with exogenous ABA application, which was suppressed by the kinase inhibitor staurosporine, indicating that an ABA-dependent post-translational modification is required for the transactivation ability of SlAREB protein. Electrophoretic mobility shift assays showed that the recombinant DNA-binding domain of SlAREB protein is able to bind AtRD29A and SlLAP promoter regions. Constitutively expressed SlAREB increased tolerance to water deficit and high salinity stresses in both Arabidopsis and tomato plants, which maintained PSII and membrane integrities as well as water content in plant bodies. Overproduction of SlAREB in Arabidopsis thaliana and tomato plants regulated stress-related genes AtRD29A, AtCOR47, and SlCI7-like dehydrin under ABA and abiotic stress treatments. Taken together, these results show that SlAREB functions to regulate some stress-responsive genes and that its overproduction improves plant tolerance to water deficit and salt stress.


ABA-responsive element binding protein Abscisic acid Salinity Water deficit 



Abscisic acid


ABA-responsive element


ABA-responsive element binding protein


Solanum lycopersicum ABA-responsive element binding protein


Responsive to dehydration 29A


Leucine aminopeptidase


Cold-induced 7

Supplementary material

425_2010_1147_MOESM1_ESM.ppt (109 kb)
Supplementary Figure S1 (PPT 109 kb)
425_2010_1147_MOESM2_ESM.doc (36 kb)
Supplementary data (DOC 36 kb)


  1. Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954–2965CrossRefPubMedGoogle Scholar
  2. Balaji V, Gibly A, Debbie P, Sessa G (2007) Transcriptional analysis of the tomato resistance response triggered by recognition of the Xanthomonas type III effecter AvrXv3. Funct Integr Genomics 7:305–316CrossRefPubMedGoogle Scholar
  3. Brini F, Hanin M, Lumbreras V, Amara I, Khoudi H, Hassairi A, Pages M, Masmoudi K (2007) Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Rep 26:2017–2026CrossRefPubMedGoogle Scholar
  4. Casaretto JA, Ho T-HD (2005) Transcriptional regulation by abscisic acid in barley (Hordeum vulgare L.) seeds involves autoregulation of the transcription factor HvABI5. Plant Mol Biol 57:21–34CrossRefPubMedGoogle Scholar
  5. Chao WS, Gu YQ, Pautot VV, Bray EA, Walling LL (1999) Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acid. Plant Physiol 120:979–992CrossRefPubMedGoogle Scholar
  6. Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  7. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236CrossRefPubMedGoogle Scholar
  8. Close TJ (1996) Dehydrins: Emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803CrossRefGoogle Scholar
  9. Douglas CJ, Ehlting J (2005) Arabidopsis thaliana full genome longmer microarrays: a powerful gene discovery tool for agriculture and forestry. Transgenic Res 14:551–561CrossRefPubMedGoogle Scholar
  10. Fei Z, Tang X, Alba RM, White JA, Ronning CM, Martin GB, Tanksley SD, Giovannoni JJ (2004) Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. Plant J 40:47–59CrossRefPubMedGoogle Scholar
  11. Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385CrossRefPubMedGoogle Scholar
  12. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, 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 17:3470–3488CrossRefPubMedGoogle Scholar
  13. Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132CrossRefPubMedGoogle Scholar
  14. 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 103:1988–1993CrossRefPubMedGoogle Scholar
  15. Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353CrossRefPubMedGoogle Scholar
  16. Hsieh TH, Lee JT, Yang PT, Chiu LH, Yy Charng, Wang YC, Chan MT (2002) Heterologous expression of the Arabidopsis C-repeat/Dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129:1086–1094CrossRefPubMedGoogle Scholar
  17. Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118CrossRefPubMedGoogle Scholar
  18. 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 7:106–111CrossRefPubMedGoogle Scholar
  19. Jouve L, Engelmann F, Noirot M, Charrier A (1993) Evaluation of biochemical markers (sugar, proline, malonedialdehyde and ethylene) for cold sensitivity in microcuttings of two coffee species. Plant Sci 91:109–116CrossRefGoogle Scholar
  20. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905CrossRefPubMedGoogle Scholar
  21. Kim S, Kang J-y, Cho D-I, 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 40:75–87CrossRefPubMedGoogle Scholar
  22. Kobayashi F, Maeta E, Terashima A, Takumi S (2008) Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings. Physiol Plant 134:74–86CrossRefPubMedGoogle Scholar
  23. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141CrossRefPubMedGoogle Scholar
  24. Liu N-Y, Ko S-S, Yeh K-C, Charng Y-Y (2006) Isolation and characterization of tomato Hsa32 encoding a novel heat-shock protein. Plant Sci 170:976–985CrossRefGoogle Scholar
  25. Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328CrossRefPubMedGoogle Scholar
  26. Luehrsen KR, de Wet J, Walbot V (1992) Transient expression analysis in plants using firefly luciferase reporter gene. Methods Enzymol 216:397–441CrossRefPubMedGoogle Scholar
  27. Mallappa C, Yadav V, Negi P, Chattopadhyay S (2006) A basic leucine zipper transcription factor, G-box-binding factor 1, regulates blue light-mediated photomorphogenic growth in Arabidopsis. J Biol Chem 281:22190–22199CrossRefPubMedGoogle Scholar
  28. Mittler R, Kim Y, Song L, Coutu J, Coutu A, Ciftci-Yilmaz S, Lee H, Stevenson B, Zhu JK (2006) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett 580:6537–6542CrossRefPubMedGoogle Scholar
  29. Mounet F, Moing A, Garcia V, Petit J, Maucourt M, Deborde C, Bernillon S, Le Gall G, Colquhoun I, Defernez M, Giraudel JL, Rolin D, Rothan C, Lemaire-Chamley M (2009) Gene and metabolite regulatory network analysis of early developing fruit tissues highlights new candidate genes for the control of tomato fruit composition and development. Plant Physiol 149:1505–1528CrossRefPubMedGoogle Scholar
  30. Mueller LA, Tanksley SD, Giovannoni JJ, van Eck J, Stack S, Choi D, Kim BD, Chen MS, Cheng ZK, Li CY, Ling HQ, Xue YB, Seymour G, Bishop Gerard, Bryan G, Sharma R, Khurana J, Tyagi A, Chattopadhyay D, Singh NK, Stiekema W, Lindhout P, Jesse T, Lankhorst RK, Bouzayen M, Shibata D, Tabata S, Granell A, Botella MA, Giuliano G, Frusciante L, Causse M, Zamir D (2005) The tomato sequencing project, the first cornerstone of the international Solanaceae project (SOL). Comp Funct Genomics 6:153–158CrossRefPubMedGoogle Scholar
  31. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  32. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325CrossRefPubMedGoogle Scholar
  33. 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 34:137–148CrossRefPubMedGoogle Scholar
  34. Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350CrossRefPubMedGoogle Scholar
  35. Oztur ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573CrossRefPubMedGoogle Scholar
  36. Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753CrossRefPubMedGoogle Scholar
  37. Rabbani MA, 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 Physiol 133:1755–1767CrossRefPubMedGoogle Scholar
  38. Rensink WA, Buell CR (2005) Microarray expression profiling resources for plant genomics. Trends Plant Sci 10:603–609CrossRefPubMedGoogle Scholar
  39. Rinne PLH, Kaikuranta PLM, van der Plas LHW, van der Schoot C (1999) Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209:377–388CrossRefPubMedGoogle Scholar
  40. Ruiz-Rivero OJ, Prat S (1998) A -308 deletion of the tomato LAP promoters is able to direct flower-specific and MeJA-induced expression in transgenic plants. Plant Mol Biol 36:639–648CrossRefPubMedGoogle Scholar
  41. Rutitzky M, Ghiglione HO, Cura JA, Casal JJ, Yanovsky MJ (2009) Comparative genomic analysis of light-regulated transcripts in the Solanaceae. BMC Genomics 10:60CrossRefPubMedGoogle Scholar
  42. Sakamoto H, Araki T, Meshi T, Iwabuchi M (2000) Expression of a subset of the Arabidopsis Cys2/His2-type zinc-finger protein gene family under water stress. Gene 248:23–32CrossRefPubMedGoogle Scholar
  43. Sanjaya, Hsiao PY, Su RC, Ko SS, Tong CG, Yang RY, Chan MT (2008) Overexpression of Arabidopsis thaliana tryptophan synthase beta 1 (AtTSB1) in Arabidopsis and tomato confers tolerance to cadmium stress. Plant Cell Environ 31:1074–1085Google Scholar
  44. Seki M, Satou M, Sakurai T, Akiyama K, Iida K, Ishida J, Nakajima M, Enju A, Narusaka M, Fujita M, Oono Y, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2004) RIKEN Arabidopsis full-length (RAFL) cDNA and its applications for expression profiling under abiotic stress conditions. J Exp Bot 55:213–223CrossRefPubMedGoogle Scholar
  45. Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223PubMedGoogle Scholar
  46. Smith DR (1996) Random primed 32P-labeling of DNA. Methods Mol Biol 58:27–29PubMedGoogle Scholar
  47. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456CrossRefPubMedGoogle Scholar
  48. Takahashi S, Seki M, Ishida J, Satou M, Sakurai T, Narusaka M, Kamiya A, Nakajima M, Enju A, Akiyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Mol Biol 56:29–55CrossRefPubMedGoogle Scholar
  49. Thurow C, Schiermeyer A, Krawczyk S, Butterbrodt T, Nickolov K, Gatz C (2005) Tobacco bZIP transcription factor TGA2.2 and related factor TGA2.1 have distinct roles in plant defense responses and plant development. Plant J 44:100–113CrossRefPubMedGoogle Scholar
  50. 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 97:11632–11637CrossRefPubMedGoogle Scholar
  51. van Berkel J, Salamini F, Gebhardt C (1994) Transcripts accumulating during cold storage of potato (Solanum tuberosum L.) tubers are sequence related to stress-responsive genes. Plant Physiol 104:445–452CrossRefPubMedGoogle Scholar
  52. Yale J, Bohnert HJ (2001) Transcript expression in Saccharomyces cerevisiae at high salinity. J Biol Chem 276:15996–16007CrossRefPubMedGoogle Scholar
  53. Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340CrossRefPubMedGoogle Scholar
  54. Yanez M, Caceres S, Orellana S, Bastias A, Verdugo I, Ruiz-Lara S, Casaretto JA (2009) An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Rep 28:1497–1507CrossRefPubMedGoogle Scholar
  55. 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 43:1473–1483CrossRefPubMedGoogle Scholar
  56. Zhang J, Kirkham MB (1994) Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791Google Scholar
  57. Zhang Y, Tessaro MJ, Lassner M, Li X (2003) Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15:2647–2653CrossRefPubMedGoogle Scholar
  58. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Tsai-Hung Hsieh
    • 1
    • 5
  • Chia-Wen Li
    • 2
  • Ruey-Chih Su
    • 3
  • Chiu-Ping Cheng
    • 4
  • Sanjaya
    • 1
    • 6
  • Yi-Chien Tsai
    • 1
    • 7
  • Ming-Tsair Chan
    • 2
  1. 1.Agricultural Biotechnology Research Center, Academia SinicaTaipeiTaiwan
  2. 2.Academia Sinica, Biotechnology Center in Southern TaiwanTainanTaiwan
  3. 3.Department of Life ScienceFu Jen Catholic UniversityTaipeiTaiwan
  4. 4.Institute of Plant BiologyNational Taiwan UniversityTaipeiTaiwan
  5. 5.Institute of Plant and Microbial Biology, Academia SinicaTaipeiTaiwan
  6. 6.Department of Biochemistry and Molecular BiologyGreat Lakes Bioenergy Research Center, MSUEast LansingUSA
  7. 7.Genomics Research Center, Academia SinicaTaipeiTaiwan

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