Skip to main content
SpringerLink
Log in

The maize heat shock factor-binding protein paralogs EMP2 and HSBP2 interact non-redundantly with specific heat shock factors

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The heat shock response (HSR) is a conserved mechanism by which transcripts of heat shock protein (hsp) genes accumulate following mobilization of heat shock transcription factors (HSFs) in response to thermal stress. Studies in animals identified the heat shock factor-binding protein1 (HSBP1) that interacts with heat shock transcription factor1 (HSF1) during heat shock attenuation; overexpression analyses revealed that the coiled-coil protein HSBP1 functions as a negative regulator of the HSR. Zea mays contains two HSBP paralogs, EMP2 and HSBP2, which exhibit differential accumulation during the HSR and plant development. Embryo-lethal recessive emp2 mutations revealed that EMP2 is required for the down-regulation of hsp transcription during embryogenesis, whereas accumulation of HSBP2 is induced in seedlings following heat shock. Notwithstanding, no interaction has yet been demonstrated between a plant HSBP and a plant HSF. In this report 22 maize HSF isoforms are identified comprising three structural classes: HSF-A, HSF-B and HSF-C. Phylogenetic analysis of Arabidopsis, maize and rice HSFs reveals that at least nine ancestral HSF isoforms were present prior to the separation of monocot and eudicots, followed by differential amplification of HSF members in these lineages. Yeast two-hybrid analyses show that EMP2 and HSBP2 interact non-redundantly with specific HSF-A isoforms. Site-specific mutagenesis of HSBP2 reveals that interactions between hydrophobic residues within the coiled coil are required for HSF::HSBP2 binding; domain swapping demonstrate that the isoform specificity of HSF::HSBP interaction is conferred by residues outside of the coiled coil. These data suggest that the non-redundant functions of the maize HSBPs may be explained, at least in part, by the specificity of HSBP::HSF interactions during plant development.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

HSR:

Heat shock response

HSF:

Heat shock factor

HSBP:

Heat shock factor-binding protein

HSP:

Heat shock protein

EMP2:

Empty pericarp2

HSBP2:

Heat shock-binding protein2

References

  • Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, Von Koskull-Doring P (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487

    Article  PubMed  CAS  Google Scholar 

  • Bharti K, Von Koskull-Doring P, Bharti S, Kumar P, Tintschl-Korbitzer A,Treuter E, Nover L (2004) Tomato heat stress transcription factor HsfB1 represents a novel type of general transcription coactivator with a histone-like motif interacting with the plant CREB binding protein ortholog HAC1. Plant Cell 16(6):1521–1535

    Article  PubMed  CAS  Google Scholar 

  • Boscheinen O, Lyck R, Queitsch C, Treuter E, Zimarino V, Scharf KD. (1997) Heat stress transcription factors from tomato can functionally replace HSF1 in the yeast Saccharomyces cerevisiae. Mol Gen Genet 255:322–331

    Article  PubMed  CAS  Google Scholar 

  • Burkhard P, Stetefeld J, Strelkov SV (2001) Coiled-coils: a highly versatile protein folding motif. Trends Cell Biol 11:82–88

    Article  PubMed  CAS  Google Scholar 

  • Busch W, Wunderlich M, Schoffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41:1–14

    Article  PubMed  CAS  Google Scholar 

  • Cotto JS, Morimoto RI (1999) Stress-induced activation of the heat-shock response: cell and molecular biology of heat-shock factors. Biochem Soc Symp 64:105–118

    PubMed  CAS  Google Scholar 

  • Cotto JS, Kline M, Morimoto RI (1996) Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation. J Biol Chem 271:3355–3358

    Article  PubMed  CAS  Google Scholar 

  • Crick FCH (1953) The packing of a-helices: simple coiled-coils. Acta Crystallogr 6:689–697

    Article  CAS  Google Scholar 

  • Czarnecka-Verner E, Yuan CX, Scharf KD, Englich G, Gurley WB (2000) Plants contain a novel multi-member class of heat shock factors without transcriptional activator potential. Plant Mol Biol 43:459–471

    Article  PubMed  CAS  Google Scholar 

  • Fu S, Meeley R, Scanlon MJ (2002) Empty pericarp2 encodes a negative regulator of the heat shock response and is required for maize embryogenesis. Plant Cell 14:3119–3132

    Article  PubMed  CAS  Google Scholar 

  • Fu S, Scanlon MJ (2004) Clonal mosaic analysis of EMPTY PERICARP2 reveals nonredundant functions of the duplicated heat shock factor binding proteins during maize shoot development. Genetics 167:1381–1394

    Article  PubMed  CAS  Google Scholar 

  • Gagliardi D, Breton C, Chaboud A, Vergne P, Dumas C (1995) Expression of heat shock factor and heat shock protein 70 genes during maize pollen development. Plant Mol Biol 4:841–856

    Article  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  PubMed  CAS  Google Scholar 

  • Ke SH, Madison EL (1997) Rapid and efficient site-directed mutagenesis by single-tube ‘megaprimer’ PCR method. Nucleic Acids Res 15:3371–3372

    Article  Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191

    Article  PubMed  CAS  Google Scholar 

  • Lohmann C, Eggers-Schumacher G, Wunderlich M, Schoffl F (2004) Two different heat shock transcription factors regulate immediate early expression of stress genes in Arabidopsis. Mol Genet Genomics 271:11–21

    Article  PubMed  CAS  Google Scholar 

  • Lupas A, Van Dyke M, Stock J (1991) Predicting coiled-coils from protein sequences. Science 252:1162–1164

    Article  PubMed  CAS  Google Scholar 

  • Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16(12):1555–1567

    Article  PubMed  CAS  Google Scholar 

  • Mosser DD, Duchaine J, Massie B (1993) The DNA-binding activity of the heat shock transcription factor is regulated in vivo by hsp70. Mol Cell Biol 13:5427–5438

    PubMed  CAS  Google Scholar 

  • Moll JR, Olive M, Vinson C (2000) Attractive interhelical electrostatic interactions in the proline- and acidic-rich region (PAR) leucine zipper subfamily preclude heterodimerization with other basic leucine zipper subfamilies. J Biol Chem 275:34826–34832

    Article  PubMed  CAS  Google Scholar 

  • Nover L, Bharti K, Doring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6:177–189

    Article  PubMed  CAS  Google Scholar 

  • Peteranderl R, Rabenstein M, Shin YK, Liu CW, Wemmer DE, King DS, Nelson HC (1999) Biochemical and biophysical characterization of the trimerization domain from the heat shock transcription factor. Biochemistry 38(12):3559–3569

    Article  PubMed  CAS  Google Scholar 

  • Peteranderl R, Nelson HC (1992)Trimerization of the heat shock transcription factor by a triple-stranded alpha-helical coiled-coil. Biochemistry 31(48):12272–12276

    Article  PubMed  CAS  Google Scholar 

  • Port M, Tripp J, Zielinski D, Weber C, Heerklotz D, Winkelhaus S, Bublak D, Scharf KD (2004) Role of Hsp17.4-CII as coregulator and cytoplasmic retention factor of tomato heat stress transcription factor HsfA2. Plant Physiol 135:1457–1470

    Article  PubMed  CAS  Google Scholar 

  • Precht H, Christophersen J, Hensel H, Larcher W (1973) Temperature and life. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Rabindran SK, Haroun RI, Clos J, Wisniewski J, Wu C (1993) Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259:230–234

    Article  PubMed  CAS  Google Scholar 

  • Ritossa F (1962) A new puffing pattern induced by heat shock and DNC in Drisophila. Experimenta 18:571–573

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2000) Molecular cloning: a laboratory manual. 3rd edn. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Sarge KD, Murphy SP, Morimoto RI (1993) Activation of heat shock gene transcription by heat shock factor1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol Cell Biol 13:1392–1407

    PubMed  CAS  Google Scholar 

  • Satyal SH, Chen D, Fox SG, Kramer JM, Morimoto RI (1998) Negative regulation of the heat shock transcriptional response by HSBP1. Genes Dev 12:1962–1974

    Article  PubMed  CAS  Google Scholar 

  • Scanlon MJ, Stinard PS, James MG, Myers AM, Robertson DS (1994) Genetic analysis of 63 mutations affecting maize kernel development isolated from Mutator stocks. Genetics 136:281–294

    PubMed  CAS  Google Scholar 

  • Scanlon MJ, Schneeberger RG, Myers AM, Freeling M (1997) The empty pericarp-2 gene is required for leaf development during maize embryogenesis. Plant J 12:901–909

    Article  CAS  Google Scholar 

  • Scharf KD, Heider H, Hohfeld I, Lyck R, Schmidt E, Nover L (1998) The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol Cell Biol 18:2240–2251

    PubMed  CAS  Google Scholar 

  • Shi Y, Mosser DD, Morimoto RI (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev 12:654–666

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Spek EJ, Bui AH, Lu M, Kallenbach NR (1998) Surface salt bridges stabilize the GCN4 leucine zipper. Protein Sci 7:2431–2437

    PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Thompson KS, Vinson CR, Freire E (1993) Thermodynamic characterization of the structural stability of the coiled-coil region of the bZIP transcription factor GCN4. Biochemistry 32:5491–5496

    Article  PubMed  CAS  Google Scholar 

  • Wolf E, Kim PS, Berger B (1997) MultiCoil: a program for predicting two- and three-stranded coiled-coils. Protein Sci 6:1179–1189

    PubMed  CAS  Google Scholar 

  • Wu C (1995) Heat shock transcription factors: structure and regulation. Ann Rev Cell Dev Biol 11:441–469

    Article  CAS  Google Scholar 

  • Wunderlich M, Werr W, Schoffl F (2003) Generation of dominant-negative effects on the heat shock response in Arabidopsis thaliana by transgenic expression of a chimaeric HSF1 protein fusion construct. Plant J 35:442–451

    Article  PubMed  CAS  Google Scholar 

  • Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K. (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci USA 99:7530–7535

    Article  PubMed  CAS  Google Scholar 

  • Yu YB (2002) Coiled-coils: stability, specificity, and drug delivery potential. Adv Drug Deliv Rev 54:1113–1129

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Mark Osterlund for technical advice in yeast genetics. This research was supported by USDA-CREES-NRICGP grant 01-01600 to MS.

Author information

Author notes

  1. Suneng Fu

    Present address: Department of Genetics and Complex Diseases, Harvard School of Public Health, Boston, MA, 02115, USA

Authors and Affiliations

  1. Plant Biology Department, University of Georgia, Athens, GA, 30602, USA

    Suneng Fu & Michael J. Scanlon

  2. Reproduction et Développement des Plantes, Institut Fédératif de Recherche, 69364, Lyon, France

    Peter Rogowsky

  3. Biocenter of the Goethe University, 60439, Frankfurt am Main, Germany

    Lutz Nover

Authors
  1. Suneng Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Rogowsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lutz Nover
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael J. Scanlon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael J. Scanlon.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fu, S., Rogowsky, P., Nover, L. et al. The maize heat shock factor-binding protein paralogs EMP2 and HSBP2 interact non-redundantly with specific heat shock factors. Planta 224, 42–52 (2006). https://doi.org/10.1007/s00425-005-0191-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0191-y

Keywords

Search

Navigation