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

Plant Molecular Biology

Volumn 58, Issue 4, 2005, Pages 543-559

  Wang, Zhibin ^a   Triezenberg, Steven J ^b   Thomashow, Michael F ^c   Stockinger, Eric J ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis; CBF DREB1 transcription factors; Cold acclimation; Mutational analysis; Transcriptional activation

Indexed keywords

AMINO ACIDS; CHEMICAL ACTIVATION; DNA; GENES; HYDROPHOBICITY; PLANTS (BOTANY); SUBSTITUTION REACTIONS; YEAST;

ARABIDOPSIS CBF PROTEINS; GENE EXPRESSION; HYDROPHOBIC MOTIFS; MUTANTS;

PROTEINS;

ARABIDOPSIS PROTEIN; BETA GLUCURONIDASE; CBF1 PROTEIN, ARABIDOPSIS; COR15 PROTEIN, ARABIDOPSIS; DNA BINDING PROTEIN; HYBRID PROTEIN; TRANSACTIVATOR PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; BINDING SITE; CHEMISTRY; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HYDROPHOBICITY; METABOLISM; MOLECULAR GENETICS; MUTATION; PHENOTYPE; PROMOTER REGION; PROTEIN MOTIF; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRANSACTIVATION; TRANSGENIC PLANT;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; GLUCURONIDASE; HYDROPHOBICITY; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS (GENETICS); RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS;

ACTIVATION; AMINO ACIDS; GENES; NUCLEIC ACIDS; PLANTS; PROTEINS; WATER REPELLENCE; YEASTS;

ARABIDOPSIS;

EID: 23744469718     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-005-6760-4     Document Type: Article

References (60)

1. Arabidopsis Genome Initiative 2000 Analysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature 408 796 815
2. Artus 1996 Constitutive 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
3. 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
4. S.S. Baker K.S. Wilhelm M.F. Thomashow 1994 The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression Plant Mol. Biol. 24 701 713
5. W.M. Barnes 1990 Variable patterns of expression of luciferase in transgenic tobacco leaves Proc. Natl. Acad. Sci. USA 87 9183 9187
6. N. Bechtold J. Ellis G. Pelletier 1993 In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants C R Acad. Sci. Ser. III Life Sci. 316 1194 1199
7. S.L. Berger B. Pina N. Silverman G.A. Marcus J. Agapite J.L. Regier S.J. Triezenberg L. Guarente 1992 Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains Cell 70 251 265
8. I. Callebaut G. Labesse P. Durand A. Poupon L. Canard J. Chomilier B. Henrissat J.P. Mornon 1997 Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives Cell Mol. Life Sci. 53 621 645
9. D.W. Choi E.M. Rodriguez T.J. Close 2002 Barley Cbf3 gene identification, expression pattern, and map location Plant Physiol. 129 1781 1787
10. S.J. Clough A.F. Bent 1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Plant J 16 735 743
11. W.D. Cress S.J. Triezenberg 1991 Critical structural elements of the VP16 transcriptional activation domain Science 251 87 90
12. B.C. Cunningham J.A. Wells 1989 High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis Science 244 1081 1085
13. P. Doring E. Treuter C. Kistner R. Lyck A. Chen L. Nover 2000 The role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2 Plant Cell 12 265 278
14. C.M. Drysdale E. Duenas B.M. Jackson U. Reusser G.H. Braus A.G. Hinnebusch 1995 The transcriptional activator GCN4 contains multiple activation domains that are critically dependent on hydrophobic amino acids Mol. Cell Biol. 15 1220 1233
15. J.G. Dubouzet Y. Sakuma Y. Ito M. Kasuga E.G. Dubouzet S. Miura M. Seki K. Shinozaki K. Yamaguchi-Shinozaki 2003 OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression Plant J 33 751 763
16. T. Durfee K. Becherer P.L. Chen S.H. Yeh Y. Yang A.E. Kilburn W.H. Lee S.J. Elledge 1993 The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit Genes Dev 7 555 569
17. A.P. Feinberg B. Vogelstein 1983 A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity Anal. Biochem. 132 6 13
18. S. Fowler M.F. Thomashow 2002 Arabidopsis 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
19. M.J. Gao G. Allard L. Byass A.M. Flanagan J. Singh 2002 Regulation and characterization of four CBF transcription factors from Brassica napus Plant Mol. Biol. 49 459 471
20. S.J. Gilmour S.G. Fowler M.F. Thomashow 2004 Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities Plant Mol. Biol. 54 767 781
21. S.J. Gilmour A.M. Sebolt M.P. Salazar J.D. Everard M.F. Thomashow 2000 Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation Plant Physiol. 124 1854 1865
22. S.J. Gilmour D.G. Zarka E.J. Stockinger M.P. Salazar J.M. Houghton M.F. Thomashow 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. 16 433 442
23. E. Giniger S.M. Varnum M. Ptashne 1985 Specific DNA binding of GAL4, a positive regulatory protein of yeast Cell 40 767 774
24. V. Haake D. Cook J.L. Riechmann O. Pineda M.F. Thomashow J.Z. Zhang 2002 Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis Plant Physiol. 130 639 648
25. J.W. Harper G.R. Adami N. Wei K. Keyomarsi S.J. Elledge 1993 The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases Cell 75 805 816
26. 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 Plant Molecular Biology Manual Kluwer Dordrecht, The Netherlands 1 11
27. B.M. Jackson C.M. Drysdale K. Natarajan A.G. Hinnebusch 1996 Identification of seven hydrophobic clusters in GCN4 making redundant contributions to transcriptional activation Mol. Cell Biol. 16 5557 5571
28. K.R. Jaglo-Ottosen S.J. Gilmour D.G. Zarka O. Schabenberger M.F. Thomashow 1998 Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance Science 280 104 106
29. K.R. Jaglo S. Kleff K.L. Amundsen X. Zhang V. Haake J.Z. Zhang T. Deits M.F. Thomashow 2001 Components 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
30. R.A. Jefferson K.J. Wilson 1991 The GUS gene fusion system S. Gelvin R. Schilperoort Plant Molecular Biology Manual Kluwer Dordrecht, The Netherlands 11 33
31. T.M. Klein M. Fromm A. Weissinger D. Tomes S. Schaaf M. Sletten J.C. Sanford 1998 Transfer of foreign genes into intact maize cells with high-velocity microprojectiles Proc. Natl. Acad. Sci. USA 85 4305 4309
32. L-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
33. L. Lemesle-Varloot B. Henrissat C. Gaboriaud V. Bissery A. Morgat J.P. Mornon 1990 Hydrophobic cluster analysis: procedures to derive structural and functional information from 2-D-representation of protein sequences Biochimie 72 555 574
34. S. Li M.F. Wilkinson 1997 Site-directed mutagenesis: a two-step method using PCR and DpnI Biotechniques 23 588 590
35. C. Lin M.F. Thomashow 1992 DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15 polypeptide Plant Physiol. 99 519 525
36. Q. Liu M. Kasuga Y. Sakuma H. Abe S. Miura K. Yamaguchi-Shinozaki K. Shinozaki 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 1406
37. H. Ma M.F. Yanofsky H.J. Klee J.L. Bowman E.M. Meyerowitz 1992 Vectors for plant transformation and cosmid libraries Gene 117 161 167
38. J. Ma M. Ptashne 1987 Deletion analysis of GAL4 defines two transcriptional activating segments Cell 48 847 853
39. A.M. Metz R.T. Timmer K.S. Browning 1992 Sequences for two cDNAs encoding Arabidopsis thaliana eukaryotic protein synthesis initiation factor 4A Gene 120 313 314
40. H. Moriuchi M. Moriuchi R. Pichyangkura S.J. Triezenberg S.E. Straus J.I. Cohen 1995 Hydrophobic 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
41. M. Ptashne 1988 How eukaryotic transcriptional activators work Nature 335 683 689
42. J. Quackenbush J. Cho D. Lee F. Liang I. Holt S. Karamycheva B. Parvizi G. Pertea R. Sultana J. White 2001 The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species Nucleic Acids Res. 29 159 164
43. J.L. Regier F. Shen S.J. Triezenberg 1993 Pattern 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
44. J.L. Riechmann E.M. Meyerowitz 1998 The AP2/EREBP family of plant transcription factors Biol. Chem. 379 633 646
45. S.J. Rothstein K.N. Lahners R.J. Lotstein N.B. Carozzi S.M. Jayne D.A. Rice 1987 Promoter cassettes, antibiotic-resistance genes, and vectors for plant transformation Gene 53 153 161
46. M.B. Sainz S.A. Goff V.L. Chandler 1997 Extensive mutagenesis of a transcriptional activation domain identifies single hydrophobic and acidic amino acids important for activation in vivo Mol. Cell Biol. 17 115 122
47. E.J. Stockinger S.J. Gilmour M.F. Thomashow 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 1040
48. E.J. Stockinger Y. Mao M.K. Regier S.J. Triezenberg M.F. Thomashow 2001 Transcriptional 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
49. S.M. Sullivan P.J. Horn V.A. Olson A.H. Koop W. Niu R.H. Ebright S.J. Triezenberg 1998 Mutational analysis of a transcriptional activation region of the VP16 protein of herpes simplex virus Nucleic Acids Res. 26 4487 4496
50. M.J. Swanson H. Qiu L. Sumibcay A. Krueger S.J. Kim K. Natarajan S. Yoon A.G. Hinnebusch 2003 A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo Mol. Cell Biol. 23 2800 2820
51. S.J. Triezenberg 1995 Structure and function of transcriptional activation domains Curr. Opin. Genet. Dev. 5 190 196
52. S.J. Triezenberg R.C. Kingsbury S.L. McKnight 1988 Functional dissection of VP16, the trans-activator of herpes simplex virus immediate early gene expression Genes Dev. 2 718 729
53. T. Ulmasov Z.B. Liu G. Hagen T.J. Guilfoyle 1995 Composite structure of auxin response elements Plant Cell 7 1611 1623
54. J. Vieira J. Messing 1987 Production of single-stranded plasmid DNA Meth. Enzymol. 153 3 11
55. J.T. Vogel D.G. Zarka H.A. Van Buskirk S.G. Fowler M.F. Thomashow 2005 Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis Plant J. 41 195 211
56. S. Woodcock J.P. Mornon B. Henrissat 1992 Detection of secondary structure elements in proteins by hydrophobic cluster analysis Protein Eng. 5 629 635
57. G.P. Xue 2002 An 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
58. G.P. Xue 2003 The 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
59. D.G. Zarka J.T. Vogel D. Cook M.F. Thomashow 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. 133 910 918
60. X. Zhang S.G. Fowler H. Cheng Y. Lou S.Y. Rhee E.J. Stockinger M.F. Thomashow 2004 Freezing-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