Skip to main content
Log in

Plant homeodomain-leucine zipper I transcription factors exhibit different functional AHA motifs that selectively interact with TBP or/and TFIIB

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Different members of the HD-Zip I family of transcription factors exhibit differential AHA-like activation motifs, able to interact with proteins of the basal transcriptional machinery.

Abstract

Homeodomain-leucine zipper proteins are transcription factors unique to plants, classified in four subfamilies. Subfamily I members have been mainly associated to abiotic stress responses. Several ones have been characterized using knockout or overexpressors plants, indicating that they take part in different signal transduction pathways even when their expression patterns are similar and they bind the same DNA sequence. A bioinformatic analysis has revealed the existence of conserved motifs outside the HD-Zip domain, including transactivation AHA motifs. Here, we demonstrate that these putative activation motifs are functional. Four members of the Arabidopsis family were chosen: AtHB1, AtHB7, AtHB12 and AtHB13. All of them exhibited activation activity in yeast and in plants but with different degrees. The protein segment necessary for such activation was different for these four transcription factors as well as the role of the tryptophans they present. When interaction with components of the basal transcription machinery was tested, AtHB1 was able to interact with TBP, AtHB12 interacted with TFIIB, AtHB7 interacted with both, TBP and TFIIB while AtHB13 showed weak interactions with any of them, in yeast two-hybrid as well as in pull-down assays. Transient transformation of Arabidopsis seedlings confirmed the activation capacity and specificity of these transcription factors and showed some differences with the results obtained in yeast. In conclusion, the differential activation functionality of these transcription factors adds an important level of functional divergence of these proteins, and together with their expression patterns, these differences could explain, at least in part, their functional divergence.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AD:

Activation domain of GAL4

AHA:

Aromatic and large hydrophobic residues embedded in an acidic context

BD:

Binding domain of GAL4

CTR:

Carboxy-terminal region

HA:

Hemagglutinin

HD:

Homeodomain

HD-Zip:

Homeodomain-leucine zipper

HSF:

Heat stress transcription factor

IB:

Immunoblotting

LZ:

Leucine zipper

NTR:

Amino-terminal region

TBP:

TATA binding protein

TF:

Transcription factor

TFIIB:

Transcription factor IIB

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Aoyama T, Dong C-H, Wu Y, Carabelli M, Sessa G, Ruberti I, Morelli G, Chua N-H (1995) Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco. Plant Cell 7:1773–1785

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arce AL, Raineri J, Capella M, Cabello JV, Chan RL (2011) Uncharacterized conserved motifs outside the HD-Zip domain in HD-Zip subfamily I transcription factors; a potential source of functional diversity. BMC Plant Biol 11:42

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426

    Article  CAS  PubMed  Google Scholar 

  • Ariel F, Diet A, Verdenaud M, Gruber V, Frugier F, Chan R, Crespi M (2010) Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1. Plant Cell 22:2171–2183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren JL, Wilfred W, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:202–208

    Article  Google Scholar 

  • Cabello JV, Chan RL (2012) The homologous homeodomain-leucine zipper transcription factors HaHB1 and AtHB13 confer tolerance to drought and salinity stresses via the induction of proteins that stabilize membranes. Plant Biotech J 10:815–825

    Article  CAS  Google Scholar 

  • Cabello JV, Arce AL, Chan RL (2012) The homologous HD-Zip I transcription factors HaHB1 and AtHB13 confer cold tolerance via the induction of pathogenesis related and glucanase proteins. Plant J 69:141–153

    Article  CAS  PubMed  Google Scholar 

  • Cho S, Jang S, Chae S, Chung KM, Moon Y-H, An G, Jang SK (1999) Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol Biol 40:419–429

    Article  CAS  PubMed  Google Scholar 

  • Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • De Smet I, Lau S, Ehrismann JS, Axiotis I, Kolb M, Kientz M, Weijers D, Jürgens G (2013) Transcriptional repression of BODENLOS by HD-ZIP transcription factor HB5 in Arabidopsis thaliana. J Exp Bot 64:3009–3019

    Article  PubMed Central  PubMed  Google Scholar 

  • Döring P, Treuter E, Kistner C, Lyck R, Chen A, Nover L (2000) The role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2. Plant Cell 12:265–278

    Article  PubMed Central  PubMed  Google Scholar 

  • Gietz D, Jean AS, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20(1):425

    Google Scholar 

  • Hanson J, Johannesson H, Engström P (2001) Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HD-Zip gene ATHB13. Plant Mol Biol 2:247–262

    Article  Google Scholar 

  • Henriksson E, Olsson ASB, Johannesson H, Johansson H, Hanson J, Engstrom P, Söderman E (2005) Homeodomain leucine zipper Class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 139:509–518

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Higuchi R, Krummel B, Saiki RK (1988) A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16:7351–7367

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hofer J, Turner L, Moreau C, Ambrose M, Isaac P, Butcher S, Weller J, Dupin A, Dalmais M, Le Signor C, Bendahmane A, Ellis N (2009) Tendril-less regulates tendril formation in pea leaves. Plant Cell 21:420–428

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ingles CJ, Shales M, Cress WD, Triezenberg SJ, Greenblatt J (1991) Reduced binding of TFIID to transcriptionally compromised mutants of VP16. Nature 351:588–590

    Article  CAS  PubMed  Google Scholar 

  • Johannesson H, Wang Y, Engström P (2001) DNA-binding and dimerization preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro. Plant Mol Biol 45:63–73

    Article  CAS  PubMed  Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298

    Article  CAS  PubMed  Google Scholar 

  • Kotak S, Port M, Ganguli A, Bicker F, von Koskull-Döring P (2004) Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J 39:98–112

    Article  CAS  PubMed  Google Scholar 

  • Kushnirov VV (2000) Rapid and reliable protein extraction from yeast. Yeast 16:857–860

    Article  CAS  PubMed  Google Scholar 

  • Lee Y-H, Oh H-S, Cheon C-I, Hwang I-T, Kim Y-J, Chun J-Y (2001) Structure and expression of the Arabidopsis thaliana homeobox gene Athb-12. Biochem Biophys Res Commun 284:133–141

    Article  CAS  PubMed  Google Scholar 

  • Li J-F, Park E, von Arnim AG, Nebenführ A (2009) The FAST technique: a simplified Agrobacterium-based transformation method for transient gene expression analysis in seedlings of Arabidopsis and other plant species. Plant Methods 5:6

    Article  PubMed Central  PubMed  Google Scholar 

  • Lin YS, Ha I, Maldonado E, Reingberg D, Green MR (1991) Binding of general transcription factor TFIIB to an acidic activation region. Nature 353:569–571

    Article  CAS  PubMed  Google Scholar 

  • Meijer AH, de Kam RJ, d’Erfurth I, Shen W, Hoge JHC (2000) HD-Zip proteins of families I and II from rice: interactions and functional properties. Mol Gen Genet 263:12–21

    Article  CAS  PubMed  Google Scholar 

  • Mitsuda N, Ohme-Takagi M (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol 50:1232–1348

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ohta M, Ohme-Takagi M, Shinshi H (2000) Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. Plant J 22:29–38

    Article  CAS  PubMed  Google Scholar 

  • Olsson ASB, Engström P, Söderman E (2004) The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis. Plant Mol Biol 55:663–677

    Article  CAS  PubMed  Google Scholar 

  • Palena CM, Gonzalez DH, Chan RL (1999) A monomer-dimer equilibrium modulates the interaction of the sunflower homeodomain leucine-zipper protein Hahb-4 with DNA. Biochem J 341:81–87

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pugh BF (1996) Mechanisms of transcription complex assembly. Curr Opin Cell Biol 8:303–311

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-Z, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  CAS  PubMed  Google Scholar 

  • Ruberti I, Sessa G, Lucchetti S, Morelli G (1991) A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J 10:1787–1791

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sakuma S, Pourkheirandish M, Matsumoto T, Koba T, Komatsuda T (2010) Duplication of a well-conserved homeodomain-leucine zipper transcription factor gene in barley generates a copy with more specific functions. Funct Integr Genomics 10:123–133

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sakuma S, Pourkheirandish M, Hensel G, Kumlehn J, Stein N, Tagiri A, Yamaji N, Ma JF, Sassa H, Koba T, Komatsuda T (2013) Divergence of expression pattern contributed to neofunctionalization of duplicated HD-Zip I transcription factor in barley. New Phytol 197:939–948

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen F, Triezenberg SJ, Hensley P, Porter D, Knutson JR (1996) Transcriptional activation domain of the herpexvirus protein VP16 becomes conformationally constrained upon interaction with basal transcription factors. J Biol Chem 271:4827–4837

    Article  CAS  PubMed  Google Scholar 

  • Sherman F, Wakem P (1991) Getting started with yeast. Methods Enzymol 194:3–21

    Article  CAS  PubMed  Google Scholar 

  • Söderman E, Mattsson J, Engström P (1996) The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J 10:375–381

    Article  PubMed  Google Scholar 

  • Son O, Hur YS, Kim YK, Lee HJ, Kim S, Kim MR, Nam KH, Lee MS, Kim BY, Park J, Park J, Lee SC, Hanada A, Yamaguchi S, Lee IJ, Kim SK, Yun DJ, Söderman E, Cheon CI (2010) ATHB12, an ABA-inducible homeodomain-leucine zipper (HD-Zip) protein of Arabidopsis, negatively regulates the growth of the inflorescence stem by decreasing the expression of a gibberellin 20-oxidase gene. Plant Cell Physiol 51:1537–1547

    Article  CAS  PubMed  Google Scholar 

  • Stringer KF, Ingles CJ, Greenblatt J (1990) Direct and selective binding of an acidic transcriptional activation domain to the TATA-box factor TFIID. Nature 345:783–786

    Article  CAS  PubMed  Google Scholar 

  • Treuter E, Nover L, Ohme K, Scharf K-D (1993) Promoter specificity and deletion analysis of three heat stress transcription factors of tomato. Mol Gen Genet 240:113–125

    Article  CAS  PubMed  Google Scholar 

  • Venters BJ, Pugh F (2009) How eukaryotic genes are transcribed. Crit Rev Biochem Mol Biol 44:117–141

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang YJ, Li YD, Luo GZ, Tian AG, Wang HW, Zhang JS, Chen SY (2005) Cloning and characterization of an HDZip I gene GmHZ1 from soybean. Planta 221:831–843

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191–203

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Haider I, Kohlen W, Jiang L, Bouwmeester H, Meijer AH, Schluepmann H, Liu C-M, Ouwerkerk PBF (2012) Function of the HD-Zip I gene Oshox22 in ABA-mediated drought and salt tolerances in rice. Plant Mol Biol 80:571–585

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Agencia Nacional de Promoción Científica y Tecnológica (PICT 2008 1206, PICT 2011 0859 and PICT 2012 0955), and Universidad Nacional del Litoral (UNL). MC, DAR are CONICET Ph.D. Fellows, ALA is a post-doctoral Fellow of the same institution and RLC is a CONICET Career member.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raquel L. Chan.

Additional information

Communicated by K. Kamo.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Capella, M., Ré, D.A., Arce, A.L. et al. Plant homeodomain-leucine zipper I transcription factors exhibit different functional AHA motifs that selectively interact with TBP or/and TFIIB. Plant Cell Rep 33, 955–967 (2014). https://doi.org/10.1007/s00299-014-1576-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-014-1576-9

Keywords

Navigation