Abstract
A subset of homeodomain leucine zipper proteins (HDZip) play a role in regulating adaptation responses including developmental adjustment to environmental cues in plants. Here we report the structural and functional characterisation of a dehydration responsive nuclear-targeted HDZip transcriptional regulator, CpHB-7. DNA–protein interaction studies suggest that CDeT6-19, a known ABA and dehydration responsive dehydrin gene, is a potential target gene of CpHB-7 in the desiccation-tolerant plant Craterostigma plantagineum. Transgenic plants that ectopically express CpHB-7 display reduced sensitivity towards ABA during seed germination and stomatal closure. Expression analysis reveals that genes with induced or repressed expression in CpHB-7 ectopic expression lines are either mostly repressed or induced by ABA, drought or salt treatment respectively, thus demonstrating that CpHB-7 modifies ABA-responsive gene expression as a negative regulator. CpHB-7 gene expression is also linked to early organ development, leading to the suggestion that CpHB-7 is functionally similar to the Arabidopsis transcription factor, ATHB-6.
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References
G.J. Allen S.P. Chu C.L. Harrington K. Schumacher T. Hoffmann Y.Y. Tang E. Grill J.I Schroeder (2001) ArticleTitleA defined range of guard cell calcium oscillation parameters encodes stomatal movements Nature 411 1053–1057 Occurrence Handle11429606 Occurrence Handle1:CAS:528:DC%2BD3MXltVCru7w%3D Occurrence Handle10.1038/35082575
S. Baima M. Possenti A. Matteucci E. Wisman M.M. Altamura I. Ruberti G. Morelli (2001) ArticleTitleThe Arabidopsis ATHB-8 HD-Zip protein acts as a differentiation-promoting transcription factor of the vascular meristems Plant Physiol. 126 643–655 Occurrence Handle11402194 Occurrence Handle1:CAS:528:DC%2BD3MXks1Gmsrs%3D Occurrence Handle10.1104/pp.126.2.643
D. Bartels R. Sunkar (2005) ArticleTitleDrought and salt tolerance in plants Crit. Rev. Plant Sci. 24 23–58 Occurrence Handle1:CAS:528:DC%2BD2MXis12ns7c%3D
D. Bartels K. Schneider G. Terstappen D. Piatkowski F. Salamini (1990) ArticleTitleMolecular cloning of abscisic acid modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum Planta 181 27–34 Occurrence Handle1:CAS:528:DyaK3cXksFelsrg%3D Occurrence Handle10.1007/BF00202321
D. Bellin M. Werber T. Theis B. Weisshaar K. Schneider (2002) ArticleTitleEST sequencing, annotation and macroarray transcriptome analysis identify preferentially expressed genes in sugar beet Plant Biol. 4 700–710 Occurrence Handle1:CAS:528:DC%2BD3sXis1elu7g%3D Occurrence Handle10.1055/s-2002-37405
M.M. Bradford (1976) ArticleTitleA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 248–254 Occurrence Handle942051 Occurrence Handle1:CAS:528:DyaE28XksVehtrY%3D Occurrence Handle10.1016/0003-2697(76)90527-3
T.R. Burglin (1997) ArticleTitleAnalysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals Nucl. Acids Res. 25 4173–4180 Occurrence Handle9336443 Occurrence Handle1:CAS:528:DyaK2sXns1Grtr4%3D Occurrence Handle10.1093/nar/25.21.4173
S.J. Clough A.F. Bent (1998) ArticleTitleFloral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Plant J. 16 735–743 Occurrence Handle10069079 Occurrence Handle1:STN:280:DyaK1M7mvVagsQ%3D%3D Occurrence Handle10.1046/j.1365-313x.1998.00343.x
S. Cutler M. Ghassemian D. Bonetta S. Cooney P. McCourt (1996) ArticleTitleA protein farnesyltransferase involved in abscisic acid signal transduction in Arabidopsis Science 273 1239–1241 Occurrence Handle8703061 Occurrence Handle1:CAS:528:DyaK28Xltlajs74%3D
X. Deng J. Phillips A.H. Meijer F. Salamini D. Bartels (2002) ArticleTitleCharacterization of five novel dehydration-responsive homeodomain leucine zipper genes from the resurrection plant Craterostigma plantagineum Plant Mol. Biol. 49 601–610 Occurrence Handle12081368 Occurrence Handle1:CAS:528:DC%2BD38XkvVWru7w%3D Occurrence Handle10.1023/A:1015501205303
R.R. Finkelstein S.S.L. Gampala C.D. Rock (2002) ArticleTitleAbscisic acid signaling in seeds and seedlings Plant Cell 14 S15–S45 Occurrence Handle12045268 Occurrence Handle1:CAS:528:DC%2BD38XksV2htbc%3D
R.R. Finkelstein (1994) ArticleTitleMutations at two new Arabidopsis ABA response loci are similar to the abi3 mutation Plant J. 5 765–771 Occurrence Handle10.1046/j.1365-313X.1994.5060765.x
W. Frank J. Phillips F. Salamini D. Bartels (1998) ArticleTitleTwo dehydration-inducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins Plant J. 15 413–421 Occurrence Handle9750352 Occurrence Handle1:CAS:528:DyaK1cXlvV2gt7w%3D Occurrence Handle10.1046/j.1365-313X.1998.00222.x
A. Furini C. Koncz F. Salamini D. Bartels (1994) ArticleTitleAgrobacterium-mediated transformation of the desiccation tolerant plant Craterostigma plantagineum Plant Cell Rep. 14 102–106 Occurrence Handle1:CAS:528:DyaK2MXjvFGns74%3D Occurrence Handle10.1007/BF00233770
J. Garcia-Bustos J. Heitman M.N. Hall (1991) ArticleTitleNuclear protein localization Biochem. Biophys. Acta 1071 83–101 Occurrence Handle2004116 Occurrence Handle1:CAS:528:DyaK3MXhsF2hsr8%3D
W.J. Gehring Y.Q. Qian M. Billeter K. Furukubo-Tokunaka A.F. Schier D. Resendez-Perez M. Affolter G. Otting K. Wuthrich (1994) ArticleTitleHomeodomain-DNA recognition Cell 78 211–223 Occurrence Handle8044836 Occurrence Handle1:CAS:528:DyaK2cXlt1KitLc%3D Occurrence Handle10.1016/0092-8674(94)90292-5
Gerlach, W.L. and Bedbrook, J.R. 1979. Cloning and charactrisation of ribosomal RNA genes from wheat and barley. Nucl. Acids Res. 7: 1869–1885
D. Görlich I.W. Mattaj (1996) ArticleTitleNucleocytoplasmic transport Science 271 1513–1518 Occurrence Handle8599106
J. Hanson H. Johannesson P. Engstrom (2001) ArticleTitleSugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZip gene ATHB13 Plant Mol. Biol. 45 247–262 Occurrence Handle11292072 Occurrence Handle1:CAS:528:DC%2BD3MXis1Kgtrg%3D Occurrence Handle10.1023/A:1006464907710
E. Henriksson A.S.B. Olsson H. Johannesson H. Johansson J. Hanson P. Engström E. Söderman (2005) ArticleTitleHomeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships Plant Physiol. 139 509–518 Occurrence Handle16055682 Occurrence Handle1:CAS:528:DC%2BD2MXhtVCgurrE Occurrence Handle10.1104/pp.105.063461
A. Himmelbach T. Hoffmann M. 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 Handle12065416 Occurrence Handle1:CAS:528:DC%2BD38XlsVSltb0%3D Occurrence Handle10.1093/emboj/cdf316
L.D. Holappa M.K. Walker-Simmons (1995) ArticleTitleThe wheat abscisic acid-responsive protein kinase mRNA, PKABA1, is up-regulated by dehydration, cold temperature, and osmotic stress Plant Physiol. 108 1203–1210 Occurrence Handle12228537 Occurrence Handle1:CAS:528:DyaK2MXmvFGmurk%3D
R.B. Horsch J.E. Fry N.L. Hoffmann D. Eichholtz S.G. Rogers R.T. Fraley (1985) ArticleTitleA simple and general method for transferring genes into plants Science 227 1229–1231 Occurrence Handle1:CAS:528:DyaL2MXhtFSjsLc%3D
H. Johannesson Y. Wang P. Engstrom (2001) ArticleTitleDNA-binding and dimerization preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro Plant Mol. Biol. 45 63–73 Occurrence Handle11247607 Occurrence Handle1:CAS:528:DC%2BD3MXhvVeku7o%3D Occurrence Handle10.1023/A:1006423324025
H. Johannesson Y. Wang J. Hanson P. Engstrom (2003) ArticleTitleThe Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings Plant Mol. Biol. 51 719–729 Occurrence Handle12678559 Occurrence Handle1:CAS:528:DC%2BD3sXhsVWjt7s%3D Occurrence Handle10.1023/A:1022567625228
Kirch, H.H., Phillips, J. and Bartels, D.,2002. Dehydration stress signal transduction. In: D. Scheel and C. Wasternack (Eds.), Plant Signal Transduction: Frontiers in Molecular Biology, Oxford University Press, pp. 140–164
Y. Kobayashi S. Yamamoto H. Minami Y. Kagaya T. Hattori (2004) ArticleTitleDifferential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid Plant Cell 16 1163–1177 Occurrence Handle15084714 Occurrence Handle1:CAS:528:DC%2BD2cXktlOqsb4%3D Occurrence Handle10.1105/tpc.019943
M. Koornneef G. Reuling C. Karssen (1984) ArticleTitleThe isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana Physiol. Plant 61 377–383 Occurrence Handle1:CAS:528:DyaL2cXltVOmtr8%3D Occurrence Handle10.1111/j.1399-3054.1984.tb06343.x
Y. Lee H. Oh C. Cheon I. Hwang Y. Kim J. Chun (2001) ArticleTitleStructure and expression of the Arabidopsis thaliana homeobox gene Athb-12 Biochem. Biophys. Res. Commun. 284 133–141 Occurrence Handle11374882 Occurrence Handle1:CAS:528:DC%2BD3MXjslyisbY%3D Occurrence Handle10.1006/bbrc.2001.4904
J. Leung J. Giraudat (1998) ArticleTitleAbscisic acid signal transduction Ann. Rev. Plant Physiol. Plant Mol. Biol. 49 199–222 Occurrence Handle1:CAS:528:DyaK1cXjvVShsb8%3D Occurrence Handle10.1146/annurev.arplant.49.1.199
J. Li X.Q. Wang M.B. Watson S.M. Assmann (2000) ArticleTitleRegulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase Science 287 300–303 Occurrence Handle10634783 Occurrence Handle1:CAS:528:DC%2BD3cXlvVWrsA%3D%3D Occurrence Handle10.1126/science.287.5451.300
A.H. Meijer E. Scarpella E.L. Dijk Particlevan L. Qin A.J. Taal S. Rueb S.E. Harrington S.R. McCouch R.A. Schilperoort J.H. Hoge (1997) ArticleTitleTranscriptional repression by Oshox1, a novel homeodomain leucine zipper protein from rice Plant J. 11 263–276 Occurrence Handle9076993 Occurrence Handle1:CAS:528:DyaK2sXitFCktb0%3D Occurrence Handle10.1046/j.1365-313X.1997.11020263.x
A.H. Meijer R.J. Kam Particlede I. d’Erfurth W. Shen J.H. Hoge (2000) ArticleTitleHD-Zip proteins of families I and II from rice: interactions and functional properties Mol. Gen. Genet. 263 12–21 Occurrence Handle10732669 Occurrence Handle1:CAS:528:DC%2BD3cXit1KgtLs%3D Occurrence Handle10.1007/PL00008671
D. Michel A. Furini F. Salamini D. Bartels (1994) ArticleTitleStructure and regulation of an ABA- and desiccation-responsive gene from the resurrection plant Craterostigma plantagineum Plant Mol. Biol. 24 549–560 Occurrence Handle8155876 Occurrence Handle1:CAS:528:DyaK2cXkslGht7s%3D Occurrence Handle10.1007/BF00023553
D. Michel F. Salamini D. Bartels P. Dale M. Baga A. Szalay (1993) ArticleTitleAnalysis of a desiccation and ABA-responsive promoter isolated from the resurrection plant Craterostigma plantagineum Plant J. 4 29–40 Occurrence Handle8220473 Occurrence Handle1:CAS:528:DyaK2cXhvVCnu7c%3D Occurrence Handle10.1046/j.1365-313X.1993.04010029.x
K. Nakai P. Horton (1999) ArticleTitlePSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization Trends Biochem. Sci. 24 34–36 Occurrence Handle10087920 Occurrence Handle1:CAS:528:DyaK1MXks12qtLk%3D Occurrence Handle10.1016/S0968-0004(98)01336-X
M. Ohgishi A. Oka G. Morelli I. Ruberti T. Aoyama (2001) ArticleTitleNegative autoregulation of the Arabidopsis homeobox gene ATHB-2 Plant J. 25 389–398 Occurrence Handle11260495 Occurrence Handle1:CAS:528:DC%2BD3MXislymt7w%3D Occurrence Handle10.1046/j.1365-313x.2001.00966.x
J.R. Phillips M.J. Oliver D. Bartels (2002) Molecular genetics of desiccation tolerant systems M. Black H.W. Pritchard (Eds) Desiccation and Survival in Plants: Drying Without Dying CABI Publishing Wallingford, UK 319–341
M. Ptashne (1988) ArticleTitleHow eukaryotic transcriptional activators work Nature 335 683–689 Occurrence Handle3050531 Occurrence Handle1:CAS:528:DyaL1cXmt1CrsLg%3D Occurrence Handle10.1038/335683a0
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 Occurrence Handle1:CAS:528:DyaK38Xht1ahu7k%3D
E. Scarpella K.J.M. Boot S. Rueb A.H. Meijer (2002) ArticleTitleThe procambium specification gene Oshox1 promotes polar auxin transport capacity and reduces its sensitivity toward inhibition Plant Physiol. 130 1349–1360 Occurrence Handle12428000 Occurrence Handle1:CAS:528:DC%2BD38XovVOms7Y%3D Occurrence Handle10.1104/pp.009167
M. Schena R.W. Davis (1994) ArticleTitleStructure of homeobox-leucine zipper genes suggests a model for the evolution of gene families Proc. Natl. Acad. Sci. USA. 91 8393–8397 Occurrence Handle7915839 Occurrence Handle1:CAS:528:DyaK2cXmt1egurc%3D Occurrence Handle10.1073/pnas.91.18.8393
M. Schena R.W. Davis (1992) ArticleTitleHD-Zip proteins: members of an Arabidopsis homeodomain superfamily Proc. Natl. Acad. Sci. USA 89 3894–3898 Occurrence Handle1349174 Occurrence Handle1:CAS:528:DyaK3sXit1yntro%3D Occurrence Handle10.1073/pnas.89.9.3894
K. Schneider B. Wells E. Schmelzer F. Salamini D. Bartels (1993) ArticleTitleDesiccation leads to the rapid accumulation of both cytosolic and chloroplastic proteins in the resurrection plant Craterostigma plantagineum hochst Planta 189 120–131 Occurrence Handle1:CAS:528:DyaK3sXls1aqsQ%3D%3D Occurrence Handle10.1007/BF00201352
J.I. Schroeder G.J. Allen V. Hugouvieux J.M. Kwak D. Waner (2001) ArticleTitleGuard cell signal transduction Ann. Rev. Plant Physiol. Plant Mol. Biol. 52 627–658 Occurrence Handle1:CAS:528:DC%2BD3MXkslWgsbc%3D Occurrence Handle10.1146/annurev.arplant.52.1.627
M. Seki M. Narusaka J. Ishida T. Nanjo M. Fujita Y. Oono A. Kamiya M. Nakajima A. Enju T. Sakurai M. Satou K. Akiyama T. Taji K. Yamaguchi-Shinozaki P. Carninci J. Kawai Y. Hayashizaki K. Shinozaki (2002) ArticleTitleMonitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray Plant J. 31 279–292 Occurrence Handle12164808 Occurrence Handle1:CAS:528:DC%2BD38XntFelsLg%3D Occurrence Handle10.1046/j.1365-313X.2002.01359.x
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 Occurrence Handle1:CAS:528:DyaK2cXpvVSgsw%3D%3D
C.J. Smith-Espinoza A.F. Richter Salamini D. Bartels (2003) ArticleTitleDissecting the response to dehydration and salt (NaCl) in the resurrection plant Craterostigma plantagineum Plant Cell Environ. 26 1307–1315 Occurrence Handle1:CAS:528:DC%2BD3sXnsVCgtLo%3D Occurrence Handle10.1046/j.0016-8025.2003.01055.x
E. Söderman M. Hjellstrom J. Fahleson P. Engstrom (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 Handle10527431 Occurrence Handle10.1023/A:1006267013170
E. Söderman J. Mattsson P. Engstrom (1996) ArticleTitleThe Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid Plant J. 10 375–381 Occurrence Handle8771791 Occurrence Handle10.1046/j.1365-313X.1996.10020375.x
R. Töpfer C. Maas C. Höricke-Grandpierre J. Schell H.-H. Steinbiss (1993) ArticleTitleExpression vectors for high-level gene expression in dicotyledonous and monocotyledonous plants Meth. Enzymol. 217 66–78 Occurrence Handle10.1016/0076-6879(93)17056-B
S.J. Triezenberg (1995) ArticleTitleStructure and function of transcriptional activation domains Curr. Opin. Genet. Develop. 5 190–196 Occurrence Handle1:CAS:528:DyaK2MXkvFWis7o%3D Occurrence Handle10.1016/0959-437X(95)80007-7
H. Wang W. Tang C. Zhu S.E. Perry (2002) ArticleTitleA chromatin immunoprecipitation (ChIP) approach to isolate genes regulated by AGL15, a MADS domain protein that preferentially accumulates in embryos Plant J. 32 831–843 Occurrence Handle12472697 Occurrence Handle1:CAS:528:DC%2BD3sXjtFWrug%3D%3D Occurrence Handle10.1046/j.1365-313X.2002.01455.x
J.Z. Zhang (2003) ArticleTitleOverexpression analysis of plant transcription factors Curr. Opin. Plant Biol. 6 430–440 Occurrence Handle12972043 Occurrence Handle1:CAS:528:DC%2BD3sXntVKhsbo%3D Occurrence Handle10.1016/S1369-5266(03)00081-5
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Xin Deng, Jonathan Phillips: These authors contributed equally to this work.
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Deng, X., Phillips, J., Bräutigam, A. et al. A Homeodomain Leucine Zipper Gene from Craterostigma plantagineum Regulates Abscisic Acid Responsive Gene Expression and Physiological Responses. Plant Mol Biol 61, 469–489 (2006). https://doi.org/10.1007/s11103-006-0023-x
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DOI: https://doi.org/10.1007/s11103-006-0023-x