Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

The Arabidopsis F-box protein TIR1 is an auxin receptor

Nature volume 435, pages 446–451 (2005)Cite this article

Abstract

Despite 100 years of evidence showing a pivotal role for indole-3-acetic acid (IAA or auxin) in plant development, the mechanism of auxin perception has remained elusive. Central to auxin response are changes in gene expression, brought about by auxin-induced interaction between the Aux/IAA transcriptional repressor proteins and the ubiquitin–ligase complex SCFTIR1, thus targeting for them proteolysis. Regulated SCF-mediated protein degradation is a widely occurring signal transduction mechanism. Target specificity is conferred by the F-box protein subunit of the SCF (TIR1 in the case of Aux/IAAs) and there are multiple F-box protein genes in all eukaryotic genomes examined so far. Although SCF–target interaction is usually regulated by signal-induced modification of the target, we have previously shown that auxin signalling involves the modification of SCFTIR1. Here we show that this modification involves the direct binding of auxin to TIR1 and thus that TIR1 is an auxin receptor mediating transcriptional responses to auxin.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Immunopurified TIR1–Myc retains the ability to interact with Aux/IAA domain II peptides in an auxin-dependent manner.
Figure 2: The association and dissociation of TIR1–Aux/IAA complexes are rapid and indicates direct auxin binding in the complex.
Figure 3: The TIR1–Aux/IAA interaction involves direct auxin binding.
Figure 4: TIR1–Myc expressed in X. laevis embryos supports auxin-enhanced interaction with Aux/IAA domain II peptides and direct auxin binding.
Figure 5: The F-box motif of TIR1 is required for auxin-induced TIR1–Aux/IAA interaction.

Similar content being viewed by others

References

  1. Leyser, O. Molecular genetics of auxin signaling. Annu. Rev. Plant Biol. 53, 377–398 (2002)

    Article  CAS  Google Scholar 

  2. Berleth, T., Krogan, N. T. & Scarpella, E. Auxin signals—turning genes on and turning cells around. Curr. Opin. Plant Biol. 7, 553–563 (2004)

    Article  CAS  Google Scholar 

  3. Friml, J. Auxin transport—shaping the plant. Curr. Opin. Plant Biol. 6, 7–12 (2003)

    Article  CAS  Google Scholar 

  4. Abel, S. & Theologis, A. Early genes and auxin action. Plant Physiol. 111, 9–17 (1996)

    Article  CAS  Google Scholar 

  5. Napier, R. M., David, K. M. & Perrot-Rechenmann, C. P. A short history of auxin-binding proteins. Plant Mol. Biol. 49, 339–348 (2002)

    Article  CAS  Google Scholar 

  6. Gray, W. M., Kepinski, S., Rouse, D., Leyser, O. & Estelle, M. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276 (2001)

    Article  ADS  CAS  Google Scholar 

  7. Zenser, N., Ellsmore, A., Leasure, C. & Callis, J. Auxin modulates the degradation rate of Aux/IAA proteins. Proc. Natl Acad. Sci. USA 98, 11795–11800 (2001)

    Article  ADS  CAS  Google Scholar 

  8. Tiwari, S. B., Wang, X.-J., Hagen, G. & Guilfoyle, T. J. AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13, 2809–2822 (2001)

    Article  CAS  Google Scholar 

  9. Tian, Q., Nagpal, P. & Reed, J. W. Regulation of Arabidopsis SHY2/IAA3 protein turnover. Plant J. 36, 643–651 (2003)

    Article  CAS  Google Scholar 

  10. Liscum, E. & Reed, J. W. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol. Biol. 49, 387–400 (2002)

    Article  CAS  Google Scholar 

  11. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Activation and repression of transcription by auxin-response factors. Proc. Natl Acad. Sci. USA 11, 5844–5849 (1999)

    Article  ADS  Google Scholar 

  12. Tiwari, S. B., Hagen, G. & Guilfoyle, T. J. Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16, 533–543 (2004)

    Article  CAS  Google Scholar 

  13. Deshaies, R. J. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 15, 435–467 (1999)

    Article  CAS  Google Scholar 

  14. Moon, J., Parry, G. & Estelle, M. The ubiquitin–proteasome pathway and plant development. Plant Cell 16, 3181–3195 (2004)

    Article  CAS  Google Scholar 

  15. Dharmasiri, N., Dharmisiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature doi:10.1038/nature03543 (this issue)

  16. Yang, X. et al. The IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1. Plant J. 40, 772–782 (2004)

    Article  CAS  Google Scholar 

  17. Gray, W. M. et al. Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev. 13, 1678–1691 (1999)

    Article  CAS  Google Scholar 

  18. Gray, W. M., Hellmann, H., Dharmasiri, S. & Estelle, M. Role of the Arabidopsis RING-H2 protein RBX1 in RUB modification and SCF function. Plant Cell 14, 2137–2144 (2002)

    Article  CAS  Google Scholar 

  19. Ruegger, M. et al. The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes Dev. 12, 198–207 (1998)

    Article  CAS  Google Scholar 

  20. Lincoln, C., Britton, J. H. & Estelle, M. Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2, 1071–1080 (1990)

    Article  CAS  Google Scholar 

  21. Ramos, J. A., Zenser, N., Leyser, O. & Callis, J. Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13, 2349–2360 (2001)

    Article  CAS  Google Scholar 

  22. Kepinski, S. & Leyser, O. Auxin-induced SCFTIR1–Aux/IAA interaction involves stable modification of the SCFTIR1 complex. Proc. Natl Acad. Sci. USA 101, 12381–12386 (2004)

    Article  ADS  CAS  Google Scholar 

  23. Dharmasiri, N., Dharmasiri, S., Jones, A. M. & Estelle, M. Auxin action in a cell-free system. Curr. Biol. 13, 1418–1422 (2003)

    Article  CAS  Google Scholar 

  24. Isaacs, H. V., Pownall, M. E. & Slack, J. M. Regulation of Hox gene expression and posterior development by the Xenopus caudal homologue Xcad3. EMBO J. 17, 3413–3427 (1998)

    Article  CAS  Google Scholar 

  25. Schulman, B. A. et al. Insights into SCF ubiquitin ligases from the structure of the Skp1–Skp2 complex. Nature 408, 381–386 (2000)

    Article  ADS  CAS  Google Scholar 

  26. Leblanc, N. et al. A novel immunological approach establishes that the auxin-binding protein, Nt-abp1, is an element involved in auxin signaling at the plasma membrane. J. Biol. Chem. 274, 28314–28320 (1999)

    Article  CAS  Google Scholar 

  27. Risseeuw, E. P. et al. Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis. Plant J. 34, 753–767 (2003)

    Article  CAS  Google Scholar 

  28. Gagne, J. M., Downes, B. P., Shiu, S. H., Durski, A. M. & Vierstra, R. D. The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl Acad. Sci. USA 99, 11519–11524 (2004)

    Article  ADS  Google Scholar 

  29. Smalle, J. & Vierstra, R. D. The ubiquitin 26s proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555–590 (2004)

    Article  CAS  Google Scholar 

  30. Semple, C. A. M. RIKEN GER Group, GSL Members. The comparative proteomics of ubiquitination in mouse. Genome Res. 13, 1389–1394 (2003)

    Article  CAS  Google Scholar 

  31. Nieuwkoop, P. D. & Faber, J. Normal Table of Xenopus laevis (Daudin) 2nd edn (North-Holland, Amsterdam, 1967)

    Google Scholar 

Download references

Acknowledgements

We thank R. Napier for invaluable advice on experimental design, numerous helpful discussions and critical reading of the manuscript; P. J. Burks and H. Isaacs for technical assistance with Xenopus expression; J. Hoggett for help with data analysis; C. Kleanthous, W. Gray, M. Estelle and T. Sieberer for discussions; and G. Sandberg and S. Day for critical reading of the manuscript. This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC).

Author information

Authors and Affiliations

  1. Department of Biology, University of York, Box 373, YO10 5YW, York, UK

    Stefan Kepinski & Ottoline Leyser

  2. Umeå Plant Science Centre, SLU, S-90183, Umeå, Sweden

    Stefan Kepinski

Authors
  1. Stefan Kepinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ottoline Leyser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Stefan Kepinski or Ottoline Leyser.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kepinski, S., Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451 (2005). https://doi.org/10.1038/nature03542

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03542

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing