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.

  • Letter
  • Published:

The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins

Nature volume 410, pages 220–223 (2001)Cite this article

Abstract

The self-incompatibility response in Brassica allows recognition and rejection of self-pollen by the stigmatic papillae. The transmembrane S-locus receptor kinase (SRK), a member of the receptor-like kinase superfamily in plants, mediates recognition of self-pollen on the female side1, whereas the S-locus cysteine-rich protein (SCR) is the male component of the self-incompatibility response2. SCR is presumably located in the pollen coat, and is thought to be the SRK ligand2,3. Although many receptor-like kinases have been isolated in plants, the mechanisms of signal transduction mediated by these molecules remain largely unknown. Here we show that SRK is phosphorylated in vivo within one hour of self-pollination. We also show that, in vitro, autophosphorylation of SRK is prevented by the stigma thioredoxin THL1 in the absence of a ligand. This inhibition is released in a haplotype-specific manner by the addition of pollen coat proteins. Our data indicate that SRK is inhibited by thioredoxins and activated by pollen coat proteins.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

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

Figure 1: SRK is phosphorylated 60 min after self-pollination in vivo, but is constitutively active in vitro.
Figure 2: Phosphorylation of SRK in vitro is inhibited by a soluble protein.
Figure 3: Thioredoxin inhibits SRK phosphorylation in vitro. a, Spirulina thioredoxin (SpTRX, 20 ng) has the same inhibitory effect as soluble stigma proteins (0.6 µg).
Figure 4: SRK is phosphorylated after adding an agonist in the presence of thioredoxin.

Similar content being viewed by others

Accession codes

Accessions

GenBank/EMBL/DDBJ

Data deposits

The GenBank accession number of BoTHL1 is AF273844.

References

  1. Takasaki, T. et al. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403, 913– 916 (2000).

    Article  ADS  CAS  Google Scholar 

  2. Schopfer, C. R., Nasrallah, M. E. & Nasrallah, J. B. The male determinant of self-incompatibility in Brassica. Science 286, 1697– 1700 (1999).

    Article  CAS  Google Scholar 

  3. Stephenson, A. G. et al. The male determinant in self-incompatibility in Brassica oleracea is located in the pollen coating. Plant J. 12, 1351– 1359 (1997).

    Article  CAS  Google Scholar 

  4. Dickinson, H. G. Dry stigmas, water and self-incompatibility in Brassica. Sex Plant Reprod. 8, 1– 10 (1995).

    Article  Google Scholar 

  5. Sarker, R. H., Elleman, C. J. & Dickinson, H. G. Control of pollen hydratation in Brassica requires continued protein synthesis and glycosylation is necessary for intraspecific incompatibility. Proc. Natl Acad. Sci. USA 85, 4340– 4344 (1988).

    Article  ADS  CAS  Google Scholar 

  6. Giranton, J. L., Dumas, C., Cock, J. M. & Gaude, T. The integral membrane S-locus receptor kinase of Brassica has serine/threonine kinase activity in a membranous environment and spontaneously forms oligomers in planta. Proc. Natl Acad. Sci. USA 97, 3759– 3764 (2000).

    Article  ADS  CAS  Google Scholar 

  7. Gu, T., Mazzurco, M., Sulaman, W., Matias, D. D. & Goring, D. R. Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc. Natl Acad. Sci. USA 95, 382– 387 (1998).

    Article  ADS  CAS  Google Scholar 

  8. Stone, S. L., Arnoldo, M. & Goring, D. R. A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286, 1729– 1731 (1999).

    Article  CAS  Google Scholar 

  9. Bower, M. S. et al. Two members of the thioredoxin-h family interact with the kinase domain of a Brassica S locus receptor kinase. Plant Cell 8, 1641– 1650 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Saitoh, M. et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17, 2596– 2606 (1998).

    Article  CAS  Google Scholar 

  11. Hashimoto, S. et al. Thioredoxin negatively regulates p38 MAP kinase activation and IL-6 production by tumor necrosis factor-α. Biochem. Biophys. Res. Commun. 258, 443– 447 (1999).

    Article  CAS  Google Scholar 

  12. Kandasamy, M. K., Paolillo, D. J., Faraday, C. D., Nasrallah, J. B. & Nasrallah, M. E. The S-locus specific glycoproteins of Brassica accumulate in the cell wall of developing stigma papillae. Dev. Biol. 134, 462– 472 (1989).

    Article  CAS  Google Scholar 

  13. Meyer, Y., Verdoucq, L. & Vignols, F. Plant thioredoxins and glutaredoxins: identity and putative roles. Trends Plant Sci. 4, 388– 394 (1999).

    Article  CAS  Google Scholar 

  14. Heldin, C. H. Dimerization of cell surface receptors in signal transduction. Cell 80, 213– 223 (1995).

    Article  CAS  Google Scholar 

  15. Spaargaren, M., Defize, L. H., Boonstra, J. & de Laat, S. W. Antibody-induced dimerization activates the epidermal growth factor receptor tyrosine kinase. J. Biol. Chem. 266, 1733– 1739 (1991).

    CAS  PubMed  Google Scholar 

  16. Delorme, V. et al. Characterization of the S locus genes, SLG and SRK, of the Brassica S 3 haplotype: identification of a membrane-localized protein encoded by the S locus receptor kinase gene. Plant J. 7, 429– 440 (1995).

    Article  CAS  Google Scholar 

  17. Gaude, T. et al. Expression of a self-incompatibility gene in a self-compatible line of Brassica oleracea. Plant Cell 5, 75– 86 (1993).

    Article  CAS  Google Scholar 

  18. Doughty, J., Hedderson, F., Mc Cubbin, A. & Dickinson, H. G. Interaction between a coating-borne peptide of the Bassica pollen grain and S (incompatibility)-locus linked stigmatic glycoproteins. Proc. Natl Acad. Sci. USA 90, 467– 471 (1993).

    Article  ADS  CAS  Google Scholar 

  19. Giranton, J. L., Ariza, M. J., Dumas, C., Cock, J. M. & Gaude, T. The S locus receptor kinase gene encodes a soluble glycoprotein corresponding to the SKR extracellular domain in Brassica oleracea. Plant J. 8, 827– 834 (1995).

    Article  CAS  Google Scholar 

  20. Flannery, A. V., Beynon, R. J. & Bond, J. S. in Proteolytic Enzymes, a Practical Approach (eds Beynon, R. J. & Bond, J. S.) 145– 162 (IRL, Oxford, 1989).

    Google Scholar 

Download references

Acknowledgements

We thank J.-L. Giranton for production of baculovirus-insect cell microsomes and A.-M. Thierry for her technical assistance. J.M.C. is a member of the Institut National de la Recherche Agronomique and T.G. is a member of the Centre National de la Recherche Scientifique.

Author information

Authors and Affiliations

  1. Reproduction et Développement des Plantes, UMR 5667 CNRS-INRA-ENSL-UCBL Ecole Normale Supérieure de Lyone, 46 Allée d’Italie, Lyon, Cedex 07 69364, France

    Didier Cabrillac, J. Mark Cock, Christian Dumas & Thierry Gaude

Authors
  1. Didier Cabrillac
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Mark Cock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Dumas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thierry Gaude
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thierry Gaude.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cabrillac, D., Cock, J., Dumas, C. et al. The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins. Nature 410, 220–223 (2001). https://doi.org/10.1038/35065626

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35065626

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