Skip to main content
SpringerLink
Log in

Multiple hydrophobic motifs in Arabidopsis CBF1 COOH-terminus provide functional redundancy in trans-activation

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The Arabidopsis CBF proteins activate expression of a set of genes whose upstream regulatory sequences typically harbor one or more copies of the CRT/DRE low temperature cis-acting DNA regulatory element. Using domain swap experiments in both yeast and Arabidopsis we show that the NH3-terminal 115 amino acids direct CBF1 to target genes and the COOH-terminal 98 amino acids function in trans-activation. Mutational analysis through the COOH-terminus using truncation and alanine-substitution mutants in yeast revealed four motifs that contribute positively towards activation. Overexpression of mutants in plants support this conclusion and also indicated that disruption of a single motif did not seriously compromise activity unless combined with the disruption of a second. These motifs consist of clusters of hydrophobic residues which are delimited from one another by short stretches of Asp, Glu, Pro and other residues favoring the formation of loops. This structural pattern is conserved across plant taxa as revealed through alignment of Arabidopsis CBF1 with homologous sequences from a diverse array of plant species. Overexpression in plants of the CBF1 COOH-terminus as a fusion with the yeast GAL4 DNA binding domain also resulted in severe stunting of growth, a phenotype which was alleviated if the activation domain was rendered ineffective. Taken together these results suggest that high level overexpression of an active, CBF activation domain compromises plant growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AD:

activation domain

CBF:

C-repeat binding factor

COR :

cold-regulated

CRT/DRE:

C-repeat/dehydration responsive element

DBD:

DNA binding domain

DREB:

dehydration responsive element binding protein

HC:

hydrophobic cluster

HCA:

hydrophobic cluster analysis

UASG:

upstream activation sequence to which the yeast GAL4 protein binds

VP16:

herpes simplex virus virion protein 16

WT:

wild type

References

  • InstitutionalAuthorNameArabidopsis Genome Initiative (2000) ArticleTitleAnalysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature 408 796–815 Occurrence Handle10.1038/35048692

    Article  Google Scholar 

  • Artus (1996) ArticleTitleConstitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance Proc.0 Natl. Acad. Sci. USA 93 13404–13409 Occurrence Handle1:CAS:528:DyaK28XmvFSnu7s%3D Occurrence Handle10.1073/pnas.93.23.13404

    Article  CAS  Google Scholar 

  • F.M. Ausubel R. Brent R.E. Kingston D.D. Moore J.G. Seidmen J.A. Smith K. Struhl (1993) Current Protocols in Molecular Biology Greene Publishing Associates/John Wiley and Sons NY

    Google Scholar 

  • S.S. Baker K.S. Wilhelm M.F. Thomashow (1994) ArticleTitleThe 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression Plant Mol. Biol. 24 701–713 Occurrence Handle1:CAS:528:DyaK2cXkslCqtrw%3D Occurrence Handle10.1007/BF00029852 Occurrence Handle8193295

    Article  CAS  PubMed  Google Scholar 

  • W.M. Barnes (1990) ArticleTitleVariable patterns of expression of luciferase in transgenic tobacco leaves Proc. Natl. Acad. Sci. USA 87 9183–9187 Occurrence Handle1:CAS:528:DyaK3MXjslSrsg%3D%3D Occurrence Handle10.1073/pnas.87.23.9183 Occurrence Handle2251262

    Article  CAS  PubMed  Google Scholar 

  • N. Bechtold J. Ellis G. Pelletier (1993) ArticleTitleIn planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants C R Acad. Sci. Ser. III Life Sci. 316 1194–1199 Occurrence Handle1:CAS:528:DyaK2cXks12hsg%3D%3D

    CAS  Google Scholar 

  • S.L. Berger B. Pina N. Silverman G.A. Marcus J. Agapite J.L. Regier S.J. Triezenberg L. Guarente (1992) ArticleTitleGenetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains Cell 70 251–265 Occurrence Handle1:CAS:528:DyaK3sXktVagsLo%3D Occurrence Handle10.1016/0092-8674(92)90100-Q Occurrence Handle1638630

    Article  CAS  PubMed  Google Scholar 

  • I. Callebaut G. Labesse P. Durand A. Poupon L. Canard J. Chomilier B. Henrissat J.P. Mornon (1997) ArticleTitleDeciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives Cell Mol. Life Sci. 53 621–645 Occurrence Handle1:CAS:528:DyaK2sXms1Clurs%3D Occurrence Handle10.1007/s000180050082 Occurrence Handle9351466

    Article  CAS  PubMed  Google Scholar 

  • D.W. Choi E.M. Rodriguez T.J. Close (2002) ArticleTitleBarley Cbf3 gene identification, expression pattern, and map location Plant Physiol. 129 1781–1787 Occurrence Handle1:CAS:528:DC%2BD38Xmtl2gt7c%3D Occurrence Handle10.1104/pp.003046 Occurrence Handle12177491 Occurrence Handle166766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Handle1:STN:280:DyaK1M7mvVagsQ%3D%3D Occurrence Handle10.1046/j.1365-313x.1998.00343.x

    Article  CAS  Google Scholar 

  • W.D. Cress S.J. Triezenberg (1991) ArticleTitleCritical structural elements of the VP16 transcriptional activation domain Science 251 87–90 Occurrence Handle1:CAS:528:DyaK3MXhtFOitL4%3D Occurrence Handle10.1126/science.1846049 Occurrence Handle1846049

    Article  CAS  PubMed  Google Scholar 

  • B.C. Cunningham J.A. Wells (1989) ArticleTitleHigh-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis Science 244 1081–1085 Occurrence Handle1:CAS:528:DyaL1MXltV2it7c%3D Occurrence Handle10.1126/science.2471267 Occurrence Handle2471267

    Article  CAS  PubMed  Google Scholar 

  • P. Doring E. Treuter C. Kistner R. Lyck A. Chen L. Nover (2000) ArticleTitleThe role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2 Plant Cell 12 265–278 Occurrence Handle1:CAS:528:DC%2BD3cXktFagtLc%3D Occurrence Handle10.1105/tpc.12.2.265 Occurrence Handle10662862 Occurrence Handle139763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • C.M. Drysdale E. Duenas B.M. Jackson U. Reusser G.H. Braus A.G. Hinnebusch (1995) ArticleTitleThe transcriptional activator GCN4 contains multiple activation domains that are critically dependent on hydrophobic amino acids Mol. Cell Biol. 15 1220–1233 Occurrence Handle1:CAS:528:DyaK2MXjsl2rsbo%3D Occurrence Handle10.1128/MCB.15.3.1220 Occurrence Handle7862116 Occurrence Handle230345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • J.G. Dubouzet Y. Sakuma Y. Ito M. Kasuga E.G. Dubouzet S. Miura M. Seki K. Shinozaki K. Yamaguchi-Shinozaki (2003) ArticleTitleOsDREB 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 Occurrence Handle1:CAS:528:DC%2BD3sXislWiu7w%3D Occurrence Handle10.1046/j.1365-313X.2003.01661.x Occurrence Handle12609047

    Article  CAS  PubMed  Google Scholar 

  • T. Durfee K. Becherer P.L. Chen S.H. Yeh Y. Yang A.E. Kilburn W.H. Lee S.J. Elledge (1993) ArticleTitleThe retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit Genes Dev 7 555–569 Occurrence Handle1:CAS:528:DyaK3sXks1Gkurk%3D Occurrence Handle10.1101/gad.7.4.555 Occurrence Handle8384581

    Article  CAS  PubMed  Google Scholar 

  • A.P. Feinberg B. Vogelstein (1983) ArticleTitleA technique for radiolabeling DNA restriction endonuclease fragments to high specific activity Anal. Biochem. 132 6–13 Occurrence Handle1:CAS:528:DyaL3sXksV2qs7c%3D Occurrence Handle10.1016/0003-2697(83)90418-9 Occurrence Handle6312838

    Article  CAS  PubMed  Google Scholar 

  • S. Fowler M.F. Thomashow (2002) ArticleTitleArabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway Plant Cell 14 1675–1690 Occurrence Handle1:CAS:528:DC%2BD38XmslChurk%3D Occurrence Handle10.1105/tpc.003483 Occurrence Handle12172015 Occurrence Handle151458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • M.J. Gao G. Allard L. Byass A.M. Flanagan J. Singh (2002) ArticleTitleRegulation and characterization of four CBF transcription factors from Brassica napus Plant Mol. Biol. 49 459–471 Occurrence Handle1:CAS:528:DC%2BD38XkvVWrurw%3D Occurrence Handle10.1023/A:1015570308704 Occurrence Handle12090622

    Article  CAS  PubMed  Google Scholar 

  • S.J. Gilmour S.G. Fowler M.F. Thomashow (2004) ArticleTitleArabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities Plant Mol. Biol. 54 767–781 Occurrence Handle1:CAS:528:DC%2BD2cXptlCrtb4%3D Occurrence Handle10.1023/B:PLAN.0000040902.06881.d4 Occurrence Handle15356394

    Article  CAS  PubMed  Google Scholar 

  • S.J. Gilmour A.M. Sebolt M.P. Salazar J.D. Everard M.F. Thomashow (2000) ArticleTitleOverexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation Plant Physiol. 124 1854–1865 Occurrence Handle1:CAS:528:DC%2BD3MXitVWqsw%3D%3D Occurrence Handle10.1104/pp.124.4.1854 Occurrence Handle11115899 Occurrence Handle59880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • S.J. Gilmour D.G. Zarka E.J. Stockinger M.P. Salazar J.M. Houghton M.F. Thomashow (1998) ArticleTitleLow temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression Plant J. 16 433–442 Occurrence Handle1:CAS:528:DyaK1MXitVensg%3D%3D Occurrence Handle10.1046/j.1365-313x.1998.00310.x Occurrence Handle9881163

    Article  CAS  PubMed  Google Scholar 

  • E. Giniger S.M. Varnum M. Ptashne (1985) ArticleTitleSpecific DNA binding of GAL4, a positive regulatory protein of yeast Cell 40 767–774 Occurrence Handle1:CAS:528:DyaL2MXktVWntLY%3D Occurrence Handle10.1016/0092-8674(85)90336-8 Occurrence Handle3886158

    Article  CAS  PubMed  Google Scholar 

  • V. Haake D. Cook J.L. Riechmann O. Pineda M.F. Thomashow J.Z. Zhang (2002) ArticleTitleTranscription factor CBF4 is a regulator of drought adaptation in Arabidopsis Plant Physiol. 130 639–648 Occurrence Handle1:CAS:528:DC%2BD38XotVKnt7o%3D Occurrence Handle10.1104/pp.006478 Occurrence Handle12376631 Occurrence Handle166593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • J.W. Harper G.R. Adami N. Wei K. Keyomarsi S.J. Elledge (1993) ArticleTitleThe p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases Cell 75 805–816 Occurrence Handle1:CAS:528:DyaK2cXhtVShsLk%3D Occurrence Handle10.1016/0092-8674(93)90499-G Occurrence Handle8242751

    Article  CAS  PubMed  Google Scholar 

  • S.H. Howell D.W. Ow M. Schneider (1989) Use of the firefly luciferase gene as a reporter of gene expression in plants S. Gelvin R. Schilperoort (Eds) Plant Molecular Biology Manual Kluwer Dordrecht, The Netherlands 1–11

    Google Scholar 

  • B.M. Jackson C.M. Drysdale K. Natarajan A.G. Hinnebusch (1996) ArticleTitleIdentification of seven hydrophobic clusters in GCN4 making redundant contributions to transcriptional activation Mol. Cell Biol. 16 5557–5571 Occurrence Handle1:CAS:528:DyaK28XlvFamur8%3D Occurrence Handle10.1128/MCB.16.10.5557 Occurrence Handle8816468 Occurrence Handle231555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • K.R. Jaglo-Ottosen S.J. Gilmour D.G. Zarka O. Schabenberger M.F. Thomashow (1998) ArticleTitleArabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance Science 280 104–106 Occurrence Handle1:CAS:528:DyaK1cXitlWrsrY%3D Occurrence Handle10.1126/science.280.5360.104 Occurrence Handle9525853

    Article  CAS  PubMed  Google Scholar 

  • K.R. Jaglo S. Kleff K.L. Amundsen X. Zhang V. Haake J.Z. Zhang T. Deits M.F. Thomashow (2001) ArticleTitleComponents of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species Plant Physiol. 127 910–917 Occurrence Handle1:CAS:528:DC%2BD3MXos1Knu7s%3D Occurrence Handle10.1104/pp.010548 Occurrence Handle11706173 Occurrence Handle129262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R.A. Jefferson K.J. Wilson (1991) The GUS gene fusion system S. Gelvin R. Schilperoort (Eds) Plant Molecular Biology Manual Kluwer Dordrecht, The Netherlands 11–33

    Google Scholar 

  • T.M. Klein M. Fromm A. Weissinger D. Tomes S. Schaaf M. Sletten J.C. Sanford (1998) ArticleTitleTransfer of foreign genes into intact maize cells with high-velocity microprojectiles Proc. Natl. Acad. Sci. USA 85 4305–4309 Occurrence Handle10.1073/pnas.85.12.4305

    Article  Google Scholar 

  • C. Koncz J. Schell (1986) ArticleTitleThe promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector Mol. Gen. Genet. 204 383–396 Occurrence Handle1:CAS:528:DyaL28XmtVeqtLk%3D Occurrence Handle10.1007/BF00331014

    Article  CAS  Google Scholar 

  • L. Lemesle-Varloot B. Henrissat C. Gaboriaud V. Bissery A. Morgat J.P. Mornon (1990) ArticleTitleHydrophobic cluster analysis: procedures to derive structural and functional information from 2-D-representation of protein sequences Biochimie 72 555–574 Occurrence Handle1:CAS:528:DyaK3MXlvVCmtw%3D%3D Occurrence Handle10.1016/0300-9084(90)90120-6 Occurrence Handle2126461

    Article  CAS  PubMed  Google Scholar 

  • S. Li M.F. Wilkinson (1997) ArticleTitleSite-directed mutagenesis: a two-step method using PCR and DpnI Biotechniques 23 588–590 Occurrence Handle1:CAS:528:DyaK2sXmslWntro%3D Occurrence Handle10.2144/97234bm05 Occurrence Handle9343667

    Article  CAS  PubMed  Google Scholar 

  • C. Lin M.F. Thomashow (1992) ArticleTitleDNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15 polypeptide Plant Physiol. 99 519–525 Occurrence Handle1:CAS:528:DyaK3sXisV2qt7k%3D Occurrence Handle10.1104/pp.99.2.519 Occurrence Handle16668917 Occurrence Handle1080494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Q. Liu M. Kasuga Y. Sakuma H. Abe S. Miura K. Yamaguchi-Shinozaki K. Shinozaki (1998) ArticleTitleTwo 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 Occurrence Handle1:CAS:528:DyaK1cXls1SisLs%3D Occurrence Handle10.1105/tpc.10.8.1391 Occurrence Handle9707537 Occurrence Handle144379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • H. Ma M.F. Yanofsky H.J. Klee J.L. Bowman E.M. Meyerowitz (1992) ArticleTitleVectors for plant transformation and cosmid libraries Gene 117 161–167 Occurrence Handle1:CAS:528:DyaK38XlsVCms7Y%3D Occurrence Handle10.1016/0378-1119(92)90725-5 Occurrence Handle1639265

    Article  CAS  PubMed  Google Scholar 

  • J. Ma M. Ptashne (1987) ArticleTitleDeletion analysis of GAL4 defines two transcriptional activating segments Cell 48 847–853 Occurrence Handle1:CAS:528:DyaL1cXltVChug%3D%3D Occurrence Handle10.1016/0092-8674(87)90081-X Occurrence Handle3028647

    Article  CAS  PubMed  Google Scholar 

  • A.M. Metz R.T. Timmer K.S. Browning (1992) ArticleTitleSequences for two cDNAs encoding Arabidopsis thaliana eukaryotic protein synthesis initiation factor 4A Gene 120 313–314 Occurrence Handle1:CAS:528:DyaK3sXkvV2hsL8%3D Occurrence Handle10.1016/0378-1119(92)90112-3 Occurrence Handle1398145

    Article  CAS  PubMed  Google Scholar 

  • H. Moriuchi M. Moriuchi R. Pichyangkura S.J. Triezenberg S.E. Straus J.I. Cohen (1995) ArticleTitleHydrophobic cluster analysis predicts an amino-terminal domain of varicella-zoster virus open reading frame 10 required for transcriptional activation Proc. Natl. Acad. Sci. USA 92 9333–9337 Occurrence Handle1:CAS:528:DyaK2MXosVWltbk%3D Occurrence Handle10.1073/pnas.92.20.9333 Occurrence Handle7568128

    Article  CAS  PubMed  Google Scholar 

  • M. Ptashne (1988) ArticleTitleHow eukaryotic transcriptional activators work Nature 335 683–689 Occurrence Handle1:CAS:528:DyaL1cXmt1CrsLg%3D Occurrence Handle10.1038/335683a0 Occurrence Handle3050531

    Article  CAS  PubMed  Google Scholar 

  • J. Quackenbush J. Cho D. Lee F. Liang I. Holt S. Karamycheva B. Parvizi G. Pertea R. Sultana J. White (2001) ArticleTitleThe TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species Nucleic Acids Res. 29 159–164 Occurrence Handle1:CAS:528:DC%2BD3MXjtlWnu7g%3D Occurrence Handle10.1093/nar/29.1.159 Occurrence Handle11125077 Occurrence Handle29813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • J.L. Regier F. Shen S.J. Triezenberg (1993) ArticleTitlePattern of aromatic and hydrophobic amino acids critical for one of two subdomains of the VP16 transcriptional activator Proc. Natl. Acad. Sci. USA 90 883–887 Occurrence Handle1:CAS:528:DyaK3sXhsVWisrY%3D Occurrence Handle10.1073/pnas.90.3.883 Occurrence Handle8381535

    Article  CAS  PubMed  Google Scholar 

  • J.L. Riechmann E.M. Meyerowitz (1998) ArticleTitleThe AP2/EREBP family of plant transcription factors Biol. Chem. 379 633–646 Occurrence Handle1:CAS:528:DyaK1cXksF2qs7Y%3D Occurrence Handle9687012

    CAS  PubMed  Google Scholar 

  • S.J. Rothstein K.N. Lahners R.J. Lotstein N.B. Carozzi S.M. Jayne D.A. Rice (1987) ArticleTitlePromoter cassettes, antibiotic-resistance genes, and vectors for plant transformation Gene 53 153–161 Occurrence Handle1:CAS:528:DyaL2sXksFensbg%3D Occurrence Handle10.1016/0378-1119(87)90003-5 Occurrence Handle3609746

    Article  CAS  PubMed  Google Scholar 

  • M.B. Sainz S.A. Goff V.L. Chandler (1997) ArticleTitleExtensive mutagenesis of a transcriptional activation domain identifies single hydrophobic and acidic amino acids important for activation in vivo Mol. Cell Biol. 17 115–122 Occurrence Handle1:CAS:528:DyaK2sXhtlWisA%3D%3D Occurrence Handle10.1128/MCB.17.1.115 Occurrence Handle8972191 Occurrence Handle231735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • E.J. Stockinger S.J. Gilmour M.F. Thomashow (1997) ArticleTitleArabidopsis 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 1035–1040 Occurrence Handle1:CAS:528:DyaK2sXhtVyhsLc%3D Occurrence Handle10.1073/pnas.94.3.1035 Occurrence Handle9023378

    Article  CAS  PubMed  Google Scholar 

  • E.J. Stockinger Y. Mao M.K. Regier S.J. Triezenberg M.F. Thomashow (2001) ArticleTitleTranscriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression Nucleic Acids Res. 29 1524–1533 Occurrence Handle1:CAS:528:DC%2BD3MXivFCgsL4%3D Occurrence Handle10.1093/nar/29.7.1524 Occurrence Handle11266554 Occurrence Handle31267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • S.M. Sullivan P.J. Horn V.A. Olson A.H. Koop W. Niu R.H. Ebright S.J. Triezenberg (1998) ArticleTitleMutational analysis of a transcriptional activation region of the VP16 protein of herpes simplex virus Nucleic Acids Res. 26 4487–4496 Occurrence Handle1:CAS:528:DyaK1cXmslynu7o%3D Occurrence Handle10.1093/nar/26.19.4487 Occurrence Handle9742254 Occurrence Handle147869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • M.J. Swanson H. Qiu L. Sumibcay A. Krueger S.J. Kim K. Natarajan S. Yoon A.G. Hinnebusch (2003) ArticleTitleA multiplicity of coactivators is required by Gcn4p at individual promoters in vivo Mol. Cell Biol. 23 2800–2820 Occurrence Handle1:CAS:528:DC%2BD3sXktV2ltro%3D Occurrence Handle10.1128/MCB.23.8.2800-2820.2003 Occurrence Handle12665580 Occurrence Handle152555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • S.J. Triezenberg (1995) ArticleTitleStructure and function of transcriptional activation domains Curr. Opin. Genet. Dev. 5 190–196 Occurrence Handle1:CAS:528:DyaK2MXkvFWis7o%3D Occurrence Handle10.1016/0959-437X(95)80007-7 Occurrence Handle7613088

    Article  CAS  PubMed  Google Scholar 

  • S.J. Triezenberg R.C. Kingsbury S.L. McKnight (1988) ArticleTitleFunctional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression Genes Dev. 2 718–729 Occurrence Handle1:CAS:528:DyaL1MXjsVCktA%3D%3D Occurrence Handle10.1101/gad.2.6.718 Occurrence Handle2843425

    Article  CAS  PubMed  Google Scholar 

  • T. Ulmasov Z.B. Liu G. Hagen T.J. Guilfoyle (1995) ArticleTitleComposite structure of auxin response elements Plant Cell 7 1611–1623 Occurrence Handle1:CAS:528:DyaK2MXovFCqurw%3D Occurrence Handle7580254 Occurrence Handle161020

    CAS  PubMed  PubMed Central  Google Scholar 

  • J. Vieira J. Messing (1987) ArticleTitleProduction of single-stranded plasmid DNA Meth. Enzymol. 153 3–11 Occurrence Handle1:CAS:528:DyaL1cXht1GgtLw%3D Occurrence Handle10.1016/0076-6879(87)53044-0 Occurrence Handle3323803

    Article  CAS  PubMed  Google Scholar 

  • J.T. Vogel D.G. Zarka H.A. Buskirk ParticleVan S.G. Fowler M.F. Thomashow (2005) ArticleTitleRoles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis Plant J. 41 195–211 Occurrence Handle1:CAS:528:DC%2BD2MXhtVWitrc%3D Occurrence Handle10.1111/j.1365-313X.2004.02288.x Occurrence Handle15634197

    Article  CAS  PubMed  Google Scholar 

  • S. Woodcock J.P. Mornon B. Henrissat (1992) ArticleTitleDetection of secondary structure elements in proteins by hydrophobic cluster analysis Protein Eng. 5 629–635 Occurrence Handle1:CAS:528:DyaK3sXhvVyhsA%3D%3D Occurrence Handle10.1093/protein/5.7.629 Occurrence Handle1480617

    Article  CAS  PubMed  Google Scholar 

  • G.P. Xue (2002) ArticleTitleAn AP2 domain transcription factor HvCBF1 activates expression of cold-responsive genes in barley through interaction with a (G/a)(C/t)CGAC motif Biochim. Biophys. Acta 1577 63–72 Occurrence Handle1:CAS:528:DC%2BD38XlvVeqsr8%3D Occurrence Handle10.1016/S0167-4781(02)00410-4 Occurrence Handle12151096

    Article  CAS  PubMed  Google Scholar 

  • G.P. Xue (2003) ArticleTitleThe DNA-binding activity of an AP2 transcriptional activator HvCBF2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature Plant J. 33 373–383 Occurrence Handle1:CAS:528:DC%2BD3sXhslWrsr8%3D Occurrence Handle10.1046/j.1365-313X.2003.01630.x Occurrence Handle12535350

    Article  CAS  PubMed  Google Scholar 

  • D.G. Zarka J.T. Vogel D. Cook M.F. Thomashow (2003) ArticleTitleCold 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. 133 910–918 Occurrence Handle1:CAS:528:DC%2BD3sXosVaqurs%3D Occurrence Handle10.1104/pp.103.027169 Occurrence Handle14500791 Occurrence Handle219064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • X. Zhang S.G. Fowler H. Cheng Y. Lou S.Y. Rhee E.J. Stockinger M.F. Thomashow (2004) ArticleTitleFreezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis Plant J. 39 905–919 Occurrence Handle1:CAS:528:DC%2BD2cXpt1GntLc%3D Occurrence Handle10.1111/j.1365-313X.2004.02176.x Occurrence Handle15341633

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Horticulture and Crop Science, The Ohio State University/OARDC, 1680 Madison Avenue, Wooster, OH, 44691, USA

    Zhibin Wang & Eric J. Stockinger

  2. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, 48824-1319, USA

    Steven J. Triezenberg

  3. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI, 48824-1312, USA

    Michael F. Thomashow

  4. Department of Crop and Soil Sciences, Michigan State University, East Lansing, MI, 48824-1325, USA

    Michael F. Thomashow

Authors
  1. Zhibin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steven J. Triezenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael F. Thomashow
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric J. Stockinger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric J. Stockinger.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Z., Triezenberg, S.J., Thomashow, M.F. et al. Multiple hydrophobic motifs in Arabidopsis CBF1 COOH-terminus provide functional redundancy in trans-activation. Plant Mol Biol 58, 543–559 (2005). https://doi.org/10.1007/s11103-005-6760-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-005-6760-4

Key words:

Search

Navigation