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Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants

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Abstract

Homeodomain-leucine zipper proteins constitute a family of transcription factors found only in plants. Hahb-4 is a member of Helianthus annuus (sunflower) subfamily I. It is regulated at the transcriptional level by water availability and abscisic acid. In order to establish if this gene plays a functional role in drought responses, transgenic Arabidopsis thaliana plants that overexpress Hahb-4 under the control of the 35S Cauliflower Mosaic Virus promoter were obtained. Transformed plants show a specific phenotype: they develop shorter stems and internodes, rounder leaves and more compact inflorescences than their non-transformed counterparts. Shorter stems and internodes are due to a lower rate in cell elongation rather than to a cell division. Transgenic plants were more tolerant to water stress conditions, showing improved development, a healthier appearance and higher survival rates than wild-type plants. Indeed, either under normal or drought conditions, they produce approximately the same seed weight per plant as wild-type plants under normal growth conditions. Plants transformed with a construct that bears the Hahb-4 promoter fused to gusA show reporter gene expression in defined cell-types and developmental stages and are induced by drought and abscisic acid. Since Hahb-4 is a transcription factor, we propose that it may participate in the regulation of the expression of genes involved in developmental responses of plants to desiccation.

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References

  • C Almoguera MA Coca J Jordano (1993) ArticleTitleTissue-specific expression of heat-shock proteins in response to water stress Plant J 4 947–958 Occurrence Handle10.1046/j.1365-313X.1993.04060947.x

    Article  Google Scholar 

  • FM Ausubel R Brent RE Kingston DD Moore JG Seidman JA Smith et al. (1983) Current Protocols in Molecular Biology John Wiley & Sons NY

    Google Scholar 

  • EA Bray (1997) ArticleTitlePlant responses to water deficit Trends Plant Sci 2 48–54 Occurrence Handle10.1016/S1360-1385(97)82562-9

    Article  Google Scholar 

  • M Carabelli G Sessa S Baima G Morelli I Ruberti (1993) ArticleTitleThe Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light Plant J 4 469–479 Occurrence Handle10.1046/j.1365-313X.1993.04030469.x Occurrence Handle8106086

    Article  PubMed  Google Scholar 

  • Carpenter CD and Simon AE (1998) Preparation of RNA. In: J Martinez-Zapater and J Salinas (eds), Arabidopsis Protocols, Methods in Molecular Biology (Vol. 82, pp. 85–89), Humana Press Inc., Totowa, NJ, USA

  • RL Chan GM Gago CM Palena DH Gonzalez (1998) ArticleTitleHomeoboxes in plant development Biochim Biophys Acta 1442 1–19 Occurrence Handle9767075

    PubMed  Google Scholar 

  • SJ Clough AF Bent (1998) ArticleTitleFloral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Plant J 16 735–743 Occurrence Handle10.1046/j.1365-313x.1998.00343.x Occurrence Handle10069079

    Article  PubMed  Google Scholar 

  • MA Coca C Almoguera TL Thomas J Jordano (1996) ArticleTitleDifferential regulation of small heat shock genes in plants: analysis of a water-stress-inducible and developmentally activated sunflower promoter Plant Mol Biol 31 863–876 Occurrence Handle10.1007/BF00019473 Occurrence Handle8806416

    Article  PubMed  Google Scholar 

  • Dixon DC and Klessig DF (1995) Immunolocalisation of proteins in fixed and embedded plant tissues. In: Maliga P, Kles-sig DF, Cashmore AR, Gruissem W and Varner JE (eds), (pp. 101-106) Cold Spring Harbor Laboratory Press.

  • JJ Doyle JL Doyle (1987) ArticleTitleA rapid DNA isolation procedure for small quantities of fresh leaf tissue Phytochem Bull 19 11–15

    Google Scholar 

  • J Fütterer T Hohn (1996) ArticleTitleTranslation in plants – rules and exceptions Plant Mol Biol 32 159–189 Occurrence Handle10.1007/BF00039382 Occurrence Handle8980479

    Article  PubMed  Google Scholar 

  • GM Gago C Almoguera J Jordano Gonzalez DH RL Chan (2002) ArticleTitleHahb-4, a homeobox leucine zipper gene potentially involved in abscisic acid-dependent responses to water stress in sunflower Plant Cell Environ 25 633–640 Occurrence Handle10.1046/j.1365-3040.2002.00853.x

    Article  Google Scholar 

  • DH González EM Valle G Gago RL Chan (1997) ArticleTitleInteraction between proteins containing homeodomains asso-ciated to leucine zippers from sunflower Biochem Biophys Acta 1351 137–149 Occurrence Handle9116027

    PubMed  Google Scholar 

  • V Haake D Cook JL Riechmann O Pineda MF Thomashow JZ Zhang (2002) ArticleTitleTranscription Factor CBF4 is a regulator of drought adaptation in Arabidopsis Plant Physiol 130 639–648 Occurrence Handle10.1104/pp.006478 Occurrence Handle12376631

    Article  PubMed  Google Scholar 

  • A Himmelbach T Hoffmann H Leube B Hohener E Grill (2002) ArticleTitleHomeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis EMBO J 21 3029–3038 Occurrence Handle10.1093/emboj/cdf316 Occurrence Handle12065416

    Article  PubMed  Google Scholar 

  • M Hjellström ASB Olsson P Engström EM Söderman (2003) ArticleTitleConstitutive expression of the water deficit-inducible homeobox gene ATHB7 in transgenic Arabidopsis causes a suppression of stem elongation growth Plant Cell Environ 26 1127–1134 Occurrence Handle10.1046/j.1365-3040.2003.01037.x

    Article  Google Scholar 

  • T-H Hsieh J-T Lee P-T Yang L-H Chiu Y-Ym Charmg Y-C Wabg M-T Chan (2002a) ArticleTitleHeterology 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 1086–1094 Occurrence Handle10.1104/pp.003442

    Article  Google Scholar 

  • T-H Hsieh J-T Lee Y-Y Charmg M-T Chan (2002b) ArticleTitleTomato plants ectopically expressing arabidopsis CBF1 show enhanced resistance to water deficit stress Plant Physiol 130 618–626 Occurrence Handle10.1104/pp.006783

    Article  Google Scholar 

  • R Höfgen L Willmtzer (1988) ArticleTitleStorage of competent cells for Agrobacterium transformation Nucl Acids Res 16 9977

    Google Scholar 

  • RA Jefferson TA Kavanagh MW Bevan (1987) ArticleTitleGUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants EMBO J 20 3901–3907

    Google Scholar 

  • H Johannesson Y Wang P Engström (2001) ArticleTitleDNA-binding and dimerisation preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro Plant Mol Biol 45 63–73 Occurrence Handle10.1023/A:1006423324025 Occurrence Handle11247607

    Article  PubMed  Google Scholar 

  • J-Y Kang H-I Choi S-Y Kim (2002) ArticleTitleArabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling Plant Cell 14 343–357 Occurrence Handle10.1105/tpc.010362 Occurrence Handle11884679

    Article  PubMed  Google Scholar 

  • M Kasuga Q Liu S Miura K Yamaguchi-Shinozaki K Shinozaki (1999) ArticleTitleImproving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor Nat Biotechnol 17 287–291 Occurrence Handle10.1038/7036 Occurrence Handle10096298

    Article  PubMed  Google Scholar 

  • M Kasuga S Miura K Shinozaki K Yamaguchi-Shinozaki (2004) ArticleTitleA 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 45 346–350 Occurrence Handle10.1093/pcp/pch037 Occurrence Handle15047884

    Article  PubMed  Google Scholar 

  • Y Kasukabe L He K Nada S Misawa I Ihara S Tachibana (2004) ArticleTitleOverexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana Plant Cell Physiol 45 712–722 Occurrence Handle10.1093/pcp/pch083 Occurrence Handle15215506

    Article  PubMed  Google Scholar 

  • JC Kim SH Lee YH Cheong CM Yoo SI Lee HJ Chun DJ Yun JC Hong SY Lee CO Lim MJ Cho (2001) ArticleTitleA novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants Plant J 25 247–259 Occurrence Handle10.1046/j.1365-313x.2001.00947.x Occurrence Handle11208017

    Article  PubMed  Google Scholar 

  • YH Lee JY Chun (1998) ArticleTitleA new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment Plant Mol Biol 37 377–384 Occurrence Handle10.1023/A:1006084305012 Occurrence Handle9617808

    Article  PubMed  Google Scholar 

  • J Leung J Giraudat (1998) ArticleTitleAbscisic acid signal transduction Annu Plant Physiol Plant Mol Biol 49 199–222 Occurrence Handle10.1146/annurev.arplant.49.1.199

    Article  Google Scholar 

  • J Mattsson E Söderman M Svenson C Borkird P Engström (1992) ArticleTitleA new homeobox-leucine zipper gene from Arabidopsis thaliana Plant Mol Biol 18 1019–1022 Occurrence Handle10.1007/BF00019223 Occurrence Handle1349836

    Article  PubMed  Google Scholar 

  • ASB Olsson P Engström E Söderman (2004) ArticleTitleThe homeobox genes ATHB7 and ATHB12 encode potential regulators of growth in response to water deficit in Arabidopsis Plant Mol Biol 55 663–677 Occurrence Handle10.1007/s11103-004-1581-4 Occurrence Handle15604708

    Article  PubMed  Google Scholar 

  • CM Palena DH Gonzalez RL Chan (1999) ArticleTitleA monomer diner equilibrium modulates the interaction of the sunflower homeodomain leucine-zipper protein Hahb-4 with DNA Biochem J 341 81–87 Occurrence Handle10.1042/0264-6021:3410081 Occurrence Handle10377247

    Article  PubMed  Google Scholar 

  • A Pellegrineschi M Reynolds M Pacheco RM Brito R Almeraya K Yamaguchi-Shinozaki D Hoisington (2004) ArticleTitleStress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions Genome 47 493–500 Occurrence Handle10.1139/g03-140 Occurrence Handle15190366

    Article  PubMed  Google Scholar 

  • AN Polidoros PV Mylona JG Scandalios (2001) ArticleTitleTransgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant–pathogen interactions and resistance to oxidative stress Trans Res 10 555–569 Occurrence Handle10.1023/A:1013027920444

    Article  Google Scholar 

  • I Ruberti G Sessa S Lucchetti G Morelli (1991) ArticleTitleA novel class of proteins containing a homeodomain with a closely linked leucine zipper motif EMBO J 10 1787–1791 Occurrence Handle1675603

    PubMed  Google Scholar 

  • M Schena RW Davis (1992) ArticleTitleHD-Zip protein members of Arabidopsis homeodomain protein superfamily Proc Natl Acad Sci USA 89 3894–3898 Occurrence Handle1349174

    PubMed  Google Scholar 

  • M Schena AM Lloyd RW Davis (1993) ArticleTitleThe HAT4 gene of Arabidopsis encodes a developmental regulator Genes Dev 7 367–379 Occurrence Handle8449400

    PubMed  Google Scholar 

  • G Sessa G Morelli I Ruberti (1993) ArticleTitleThe Athb-1 and -2 HD-Zip domains homodimerize forming complexes of different DNA binding specificities EMBO J 12 3507–3517 Occurrence Handle8253077

    PubMed  Google Scholar 

  • K Shinozaki K Yamaguchi- Shinozaki (2000) ArticleTitleMolecular responses to dehydration and low temperature: differences and cross-talk between two stress signalling pathways Curr Opin Plant Biol 3 217–223 Occurrence Handle10837265

    PubMed  Google Scholar 

  • K Shinozaki K Yamaguchi-Shinozaki (1997) ArticleTitleGene expression and signal transduction in water-stress response Plant Physiol 115 327–334 Occurrence Handle10.1104/pp.115.2.327 Occurrence Handle12223810

    Article  PubMed  Google Scholar 

  • K Skriver J Mundy (1990) ArticleTitleGene expression in response to abscisic acid and osmotic stress Plant Cell 2 503–512 Occurrence Handle10.1105/tpc.2.6.503 Occurrence Handle2152172

    Article  PubMed  Google Scholar 

  • E Söderman M Hjellström J Fahleson P Engström (1999) ArticleTitleThe HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions Plant Mol Biol 40 1073–1083 Occurrence Handle10.1023/A:1006267013170 Occurrence Handle10527431

    Article  PubMed  Google Scholar 

  • E Söderman J Mattsson P Engström (1996) ArticleTitleThe Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid Plant J 10 375–381 Occurrence Handle10.1046/j.1365-313X.1996.10020375.x Occurrence Handle8771791

    Article  PubMed  Google Scholar 

  • E Söderman J Mattsson M Svenson C Borkird P Engström (1994) ArticleTitleExpression patterns of novel genes encoding homeodomain leucine-zipper proteins in Arabidopsis thaliana Plant Mol Biol 26 145–154 Occurrence Handle10.1007/BF00039527 Occurrence Handle7948864

    Article  PubMed  Google Scholar 

  • M Suzuki T Tahahashi Y Komeda (2002) ArticleTitleFormation of Corymb-like inflorescences due to delay in bolting and flower development in the corymbosa2 mutant of Arabidopsis Plant Cell Physiol 43 298–306 Occurrence Handle10.1093/pcp/pcf036 Occurrence Handle11917084

    Article  PubMed  Google Scholar 

  • A Tilahun AC Guenzi B Martin J Cushman (2003) ArticleTitleTolerance of mannitol-accumulating transgenic wheat to water stress and salinity Plant Physiol 131 1748–1755 Occurrence Handle10.1104/pp.102.003616 Occurrence Handle12692333

    Article  PubMed  Google Scholar 

  • KU Torii N Misukawa T Oosumi Y Matsuura R Yokoyama RF Whittie Y Komeda (1996) ArticleTitleThe arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats Plant Cell 8 735–746 Occurrence Handle10.1105/tpc.8.4.735 Occurrence Handle8624444

    Article  PubMed  Google Scholar 

  • T Umezawa R Yoshida K Maruyama K Yamaguchi-Shinozaki K Shinozaki (2004) ArticleTitleSRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana Proc Natl Acad Sci USA 101 17306–17311 Occurrence Handle10.1073/pnas.0407758101 Occurrence Handle15561775

    Article  PubMed  Google Scholar 

  • Y Uno T Furihata H Abe R Yoshida K Shinozaki K Yamaguchi-Shinozaki (2000) ArticleTitleArabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions Proc Nat Acad Sci USA 97 11632–11637 Occurrence Handle10.1073/pnas.190309197 Occurrence Handle11005831

    Article  PubMed  Google Scholar 

  • D Xu X Duan B Wang B Hong T-H D Ho R Wu (1996) ArticleTitleExpression of a late embryogenesis abundant protein gene HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice Plant Physiol 110 249–257 Occurrence Handle12226181

    PubMed  Google Scholar 

  • SY Yi JH Kim YH Joung S Lee WT Kim SH Yu D Choi (2004) ArticleTitleThe pepper transcription factor CaPF1 confers pathogen and freezing tolerance m Arabidopsis Plant Physiol 136 2862–2874 Occurrence Handle10.1104/pp.104.042903 Occurrence Handle15347795

    Article  PubMed  Google Scholar 

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Correspondence to Raquel Lía Chan.

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Dezar, C.A., Gago, G.M., González, D.H. et al. Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res 14, 429–440 (2005). https://doi.org/10.1007/s11248-005-5076-0

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