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Promoter specificity and deletion analysis of three heat stress transcription factors of tomato

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Abstract

Transient expression assays in transformed tobacco (Nicotiana plumbaginifolia) mesophyll protoplasts were used to test the activity of three tomato heat stress transcription factors, HSF24, HSF8 and HSF30, in a trans-activation and a trans-repression assay. The results document differences between the three HSFs with respect to their response to the configuration of heat stress promoter elements (HSEs) in the reporter construct (promoter specificity) and to the stress regime used for activation. Analysis of C-terminal deletions identified acidic sequence elements with a central tryptophan residue, which are important for HSF activity control. Surprisingly, heterologous HSFs from Drosophila and human cells, but not from yeast, were also functional as heat stress-induced transcription factors in this tobacco protoplast system.

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References

  • Abravaya K, Phillips B, Morimoto RI (1991a) Heat shock-induced interactions of heat shock transcription factor and the human hsp70 promoter examined by in vivo footprinting. Mol Cell Biol 11:586–592

    Google Scholar 

  • Abravaya K, Phillips B, Morimoto RI (1991b) Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures. Genes Dev 5:2117–2127

    Google Scholar 

  • Abravaya K, Myers MP, Murphy SP, Morimoto RI (1992) The human heat shock protein hsp70 interacts with HSF, the transcription factor that regulates heat shock gene expression. Genes Dev 6:1153–1164

    Google Scholar 

  • Baler R, Welch WJ, Voellmy R (1992) Heat shock gene regulation by nascent polypeptides and denatured proteins — hsp70 as a potential autoregulatory factor. J Cell Biol 117:1151–1159

    Google Scholar 

  • Blackman RK, Meselson M (1986) Interspecific nucleotide sequence comparisons used to identify regulatory and structural features of the Drosophila hsp82 gene. J Mol Biol 188:499–516

    Google Scholar 

  • Carmo-Avides MD, Sunkel CE, Moradas-Ferreira P, Rodrigues-Pousada C (1990) Properties and partial characterization of the heat shock factor from Tetrahymena pyriformis. Eur J Biochem 194:331–336

    Google Scholar 

  • Clos J, Westwood JT, Becker PB, Wilson S, Lambert K, Wu C (1990) Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation. Cell 63:1085–1097

    Google Scholar 

  • Craig EA, Gross CA (1991) Is hsp70 the cellular thermometer? Trands Biochem Sci 16:135–140

    Google Scholar 

  • Dietrich PS, Bouchard RA, Casey ES, Sinibaldi RM (1991) Isolation and characterization of a small heat shock protein gene from maize. Plant Physiol 96:1268–1276

    Google Scholar 

  • Dostatni N, Lambert PE, Sousa R, Ham J, Howley PM, Janiv M (1991) The functional BPV-IE2 trans-activating protein can act as a repressor by preventing formation of the initiation complex. Genes Dev 5:1657–1671

    Google Scholar 

  • Gehring WJ (1987) Homeo boxes in the study of development. Science 236:1245–1252

    Google Scholar 

  • Goff St A, Cone VC, Chandler VL (1992) Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev 6:864–875

    Google Scholar 

  • Graham A, Papalopulu N, Krumlauf R (1989) The murine and Drosophila homcobox gene complexes have common features of organization and expression. Cell 57:367–378

    Google Scholar 

  • Jakobsen BK, Pelham HRB (1991) A conserved heptapeptide restrains the activity of the yeast heat shock transcription factor. EMBO J 10:369–375

    Google Scholar 

  • Jefferson RA (1987) Assaying chimaeric genes in plants: The gus gene fusion system. Plant Mol Biol Rep 5:387–405

    Google Scholar 

  • Katagiri F, Chua NH (1992) Plant transcription factors: present knowledge and future challenges. Trends Genet 8:22–27

    Google Scholar 

  • Krens FA, Molendijk L, Wullems GI, Schilperoort RA (1982) In vitro transformation of plant protoplasts with Ti-plasmid DNA. Nature 296:72–74

    Google Scholar 

  • Kretzner L, Blackwood EM, Eisenman RN (1992) Myc and Max proteins posses distinct transcriptional activities. Nature 359:426–429

    Google Scholar 

  • Larson JS, Schuetz TJ, Kingston RE (1988) Activation in vitro of sequence-specific DNA binding by human regulatory factor. Nature 335:372–375

    Google Scholar 

  • Menczel L, Nagy F, Kiss Z, Maliga P (1981) Streptomycin-resistant and sensitive somatic hybrids of N. tabacum + N. knightiana: Correlation of resistance to N. tabacum plastids. Theor Appl Genet 59:191–195

    Google Scholar 

  • Mosser DD, Kotzbauer PT, Sarge KD, Morimoto RI (1990) In vitro activation of heat shock transcription factor DNA-binding by calcium and biochemical conditions that effect protein conformation. Proc Natl Acad Sci USA 87:3748–3752

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Google Scholar 

  • Nagy IL, Maliga P (1976) Callus induction and plant regeneration from mesophyll protoplasts of Nicotiana sylvestris. Z Pflanzenphysiol 78:453–455

    Google Scholar 

  • Neumann D, zur Nieden U, Mantcuffel R, Walter G, Scharf KD, Nover L (1987) Intracellular localization of heat shock proteins in tomato cell cultures. Eur J Cell Biol 43:71–81

    Google Scholar 

  • Nieto-Sotelo J, Wiederrecht G, Okuda A, Parker CS (1990) The yeast heat shock transcription factor contains a transcriptional activation domain whose activity is repressed under nonshock conditions. Cell 62:807–817

    Google Scholar 

  • Nover L (1987) Expression of heat shock genes in homologous and heterologous systems. Enz Microbiol Technol 9:130–144

    Google Scholar 

  • Nover L (ed) (1991) Heat Shock Response. CRC Press, Boca Raton, Fla., USA

    Google Scholar 

  • Ogata K, Hojo H, Aimoto S, Nakai T, Nakamura H, Sarai A, Ishii S, Nishimura Y (1992) Solution structure of a DNA-binding unit myb: A helix-turn-helix-related motif with conserved tryptophans forming a hydrophobic core. Proc Natl Acad Sci USA 89:6428–6432

    Google Scholar 

  • Pelham HRB (1982) A regulatory upstream promoter element in the Drosophila Hsp70 heat-shock gene. Cell 30:517–528

    Google Scholar 

  • Rabindran SK, Giorgi G, Clos J, Wu C (1991) Molecular cloning and expression of a human heat shock factor. Proc Natl Acad Sci USA 88:6906–6910

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Sarge KD, Zimarino V, Holm K, Wu C, Morimoto RI (1991) Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA binding ability. Genes Dev 5:1902–1911

    Google Scholar 

  • Scharf KD, Rose S, Zott W, Schöffl F, Nover L (1990) Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast HSF. EMBO J 9:4495–4501

    Google Scholar 

  • Scharf KD, Rose S, Thierfelder J, Never L (1993a) Two cDNAs for tomato heat stress transcription factors. Plant Physiol, in press

  • Scharf KD, Materna T, Treuter E, Never L (1993b) Heat stress promoters and transcription factors. In Dennis E, Never L (eds.) Plant promoters and transcription factors. Springer, Berlin, in press

    Google Scholar 

  • Schena M, Davis RW (1992) HD-Zip proteins: Members of an Arabidopsis homeo domain protein superfamily. Proc Natl Acad Sci USA 89:3894–3898

    Google Scholar 

  • Schöffl R, Raschke E, Nagao RT (1984) The DNA sequence analysis of soybean heat-shock genes and identification of possible regulatory promoter elements. EMBO J 3:2491–2497

    Google Scholar 

  • Schöffl F, Rieping M, Severin K (1991) The induction of the heat shock response: Activation and expression of chimaeric heat shock genes in transgenic plants. In: Hermann RG, Larkins B (eds) Plant molecular biology, 2. Plenum Press, New York, pp 685–694

    Google Scholar 

  • Schuetz TJ, Gallo GJ, Sheldon L, Tempst P, Kingston RE (1991) Isolation of a cDNA for HSF2: Evidence for two heat shock factor genes in humans. Proc Natl Acad Sci USA 88:6911–6915

    Google Scholar 

  • Shuey DJ, Parker CS (1986) Binding of Drosophila heat-shock gene transcription factor to the hsp70 promoter. J Biol Chem 261:7934–7940

    Google Scholar 

  • Sorger PK (1990) Yeast heat shock factor contains separable transient and sustained response transcriptional activators. Cell 62:783–805

    Google Scholar 

  • Sorger PK, Pelham HRB (1988) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855–864

    Google Scholar 

  • Sorger PK, Nelson HCM (1989) Trimerization of a yeast transcriptional activator via a coiled-coil motif. Cell 59:807–813

    Google Scholar 

  • Sorger PK, Lewis MJ, Pelham HRB (1987) Heat shock factor is regulated differently in yeast and HeLa cells. Nature 329:81–84

    Google Scholar 

  • Töpfer R, Schell J, Steinbiss HH (1988) Versatile cloning vectors for transient gene expression and direct gene transfer in plant cells. Nucleic Acids Res 16:8725

    Google Scholar 

  • Weisshaar B, Armstrong GA, Block A, Costa e Silva O, Hahlbrock K (1991) Light-inducible and constitutively expressed DNA-binding proteins recognizing a plant promoter element with functional relevance to light responsiveness. EMBO J 10:1777–1786

    Google Scholar 

  • Westwood JT, Clos J, Wu C (1991) Stress-induced oligomerization and chromosomal relocalization of heat-shock factor. Nature 353:822–827

    Google Scholar 

  • Wiederrecht G, Seto D, Parker CS (1988) Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 54:841–853

    Google Scholar 

  • Xiao H, Perisic O, Lis JT (1991) Cooperative binding of Drosophila heat shock factor to arrays of a conserved 5 by unit. Cell 64:585–593

    Google Scholar 

  • Zimarino V, Wu C (1987) Induction of sequence-specific binding of Drosophila heat shock activator protein without protein synthesis. Nature 327:727–730

    Google Scholar 

  • Zimarino V, Wilson S, Wu C (1990) Antibody-mediated activation of Drosophila heat shock factor in vitro. Science 249:546–549

    Google Scholar 

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Communicated by R.G. Herrmann

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Treuter, E., Nover, L., Ohme, K. et al. Promoter specificity and deletion analysis of three heat stress transcription factors of tomato. Molec. Gen. Genet. 240, 113–125 (1993). https://doi.org/10.1007/BF00276890

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  • DOI: https://doi.org/10.1007/BF00276890

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