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 receptor kinase determines self-incompatibility in Brassica stigma

Abstract

The self-incompatibility possessed by Brassica is an intraspecific reproductive barrier by which the stigma rejects self-pollen but accepts non-self-pollen for fertilization. The molecular/biochemical bases of recognition and rejection have been intensively studied. Self-incompatibility in Brassica is sporophytically controlled by the polymorphic S locus1. Two tightly linked polymorphic genes at the S locus, S receptor kinase gene (SRK) and S locus glycoprotein gene (SLG), are specifically expressed in the papillar cells of the stigma2,3,4, and analyses of self-compatible lines5,6,7 of Brassica have suggested that together they control stigma function in self-incompatibility interactions. Here we show, by transforming self-incompatible plants of Brassica rapa with an SRK28 and an SLG 28 transgene separately, that expression of SRK28 alone, but not SLG28 alone, conferred the ability to reject self (S28)-pollen on the transgenic plants. We also show that the ability of SRK28 to reject S28 pollen was enhanced by SLG28. We conclude that SRK alone determines S haplotype specificity of the stigma, and that SLG acts to promote a full manifestation of the self-incompatibility response.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Vector construction and detection of transgenes.
Figure 2: RNA blot analysis of transcription of the endogenous SRK28 gene and the SRK28 transgene.
Figure 3: Expression of the SRK28 and SLG28 transgenes.

Similar content being viewed by others

References

  1. Bateman, A. J. Self-incompatibility systems in angiosperms. III. Cruciferae. Heredity 9, 52–68 ( 1955).

    Google Scholar 

  2. Stein, J. C. et al. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl Acad. Sci. USA 88, 8816– 8820 (1991).

    Article  ADS  CAS  Google Scholar 

  3. Takayama, S. et al. Sequences of S-glycoproteins, products of the Brassica campestris self-incompatibility locus. Nature 326 , 102–105 (1987).

    Article  ADS  CAS  Google Scholar 

  4. Nasrallah, J. B., Kao, T.-h., Chen, C.-h., Goldberg, M. L. & Nasrallah, M. E. Amino-acid sequence of glycoproteins encoded by three alleles of the S-locus of Brassica oleracea. Nature 326, 617–619 ( 1987).

    Article  ADS  CAS  Google Scholar 

  5. Goring, D. R., Glavin, T. L., Schafer, U. & Rothstein, S. J. An S receptor kinase gene in self-compatible Brassica napus has a 1-bp deletion. Plant Cell 5, 531– 539 (1993).

    Article  CAS  Google Scholar 

  6. Nasrallah, J. B., Rundle, S. J. & Nasrallah, M. E. Genetic evidence for the requirement of the Brassica S-locus receptor kinase gene in the self-incompatibility response. Plant J. 5, 373–384 ( 1994).

    Article  CAS  Google Scholar 

  7. Nasrallah, M. E., Kandasamy, M. K. & Nasrallah, J. B. A genetically defined trans-acting locus regulates S-locus function in Brassica. Plant J. 2 , 497–506 (1992).

    Article  CAS  Google Scholar 

  8. Goring, D. R. & Rothstein, S. J. The S-locus receptor kinase gene in a self-incompatible Brassica napus line encodes a functional serine/threonine kinase. Plant Cell 4, 1273 –1281 (1992).

    Article  CAS  Google Scholar 

  9. Nasrallah, J. B. & Nasrallah, M. E. Pollen–stigma signaling in the sporophytic self-incompatibility response. Plant Cell 5, 1325–1335 ( 1993).

    PubMed  PubMed Central  Google Scholar 

  10. Hinata, K., Watanabe, M., Toriyama, K. & Isogai, A. A review of recent studies on homomorphic self-incompatibility. Int. Rev. Cytol. 143, 257–296 (1993).

    Article  CAS  Google Scholar 

  11. Suzuki, G. et al. Genomic organization of the S locus: Identification and characterization of genes in SLG/SRK region of S9 haplotype of Brassica campestris (syn. rapa). Genetics 153, 391–400 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 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 

  13. Takasaki, T. et al. Introduction of SLG (S-locus glycoprotein) alters the phenotype of endogenous S-haplotype, but confers no new S-haplotype specificity in Brassica rapa L. Plant Mol. Biol. 40, 659–668 (1999).

    Article  CAS  Google Scholar 

  14. Conner, J. A. et al. Transgene-induced silencing of S-locus genes and related genes in Brassica. Plant J. 11, 809 –823 (1997).

    Article  CAS  Google Scholar 

  15. Stahl, R. J., Arnoldo, M., Glavin, T. L., Goring, D. R. & Rothstein, S. J. The self-incompatibility phenotype is altered by the transformation of a mutant S locus receptor kinase. Plant Cell 10, 209–218 (1998).

    Article  CAS  Google Scholar 

  16. Hatakeyama, K., Takasaki, T., Watanabe, M. & Hinata, K. Molecular characterization of S locus genes, SLG and SRK , in a pollen-recessive self-incompatibility haplotype of Brassica rapa L. Genetics 149, 1587– 1597 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Hatakeyama, K., Watanabe, M. Takasaki, T., Ojima, K. & Hinata, K. Dominance relationships between S alleles in self-incompatible Brassica campestris L. Heredity 80, 241–247 ( 1998).

    Article  Google Scholar 

  18. Watanabe, M. et al. A high degree of homology exists between the protein encoded by SLG and the S receptor domain encoded by SRK in self-incompatible Brassica campestris L. Plant Cell Physiol. 35, 1221–1229 (1994).

    Article  CAS  Google Scholar 

  19. Suzuki, G., Watanabe, M., Toriyama, K., Isogai, A. & Hinata, K. Expression of SLG9 and SRK9 genes in transgenic tobacco. Plant Cell Physiol. 37, 866– 869 (1996).

    Article  CAS  Google Scholar 

  20. Kish-Nishizawa, N. et al. Ultrastructure of papillar cells in Brassica campestris revealed by liquid helium rapid-freezing and substitute-fixation method. Plant Cell Physiol. 31, 1207– 1219 (1990).

    Google Scholar 

  21. 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 

  22. Suzuki, G., Watanabe, M., Toriyama, K., Isogai, A. & Hinata, K. Molecular cloning of members of the S-multigene family in self-incompatible Brassica campestris. Plant Cell Physiol. 36, 1273–1280 (1995).

    CAS  PubMed  Google Scholar 

  23. Jones, J. G. et al. Effective vectors for transformation, expression of heterologous, and assaying transposon excision in transgenic plant. Transgenic Res. 1, 285–297 ( 1992).

    Article  ADS  CAS  Google Scholar 

  24. Takasaki, T. et al. Factors influencing Agrobacterium-mediated transformation of Brassica rapa L. Breed. Sci. 47, 127–134 (1997).

    Google Scholar 

  25. Kho, Y. O. & Bear, J. Observing pollen tubes by means of fluorescence. Euphytica 17, 298– 302 (1968).

    Google Scholar 

  26. Manolson, M. F., Oucllette, B. F., Filion, M. & Poole, R. J. cDNA sequence and homologies of the ‘57-Kda’ nucleotide-binding subunit of the vacuolar ATPase from Arabidopsis. J. Biol. Chem. 263, 17987–17994 ( 1988).

    CAS  PubMed  Google Scholar 

  27. Nishio, T., Kusaba, M., Watanabe, M. & Hinata, K. Registration of S alleles in Brassica campestris L. by the restriction fragment sizes of SLGs. Theor. Appl. Genet. 92, 388–394 (1996).

    Article  CAS  Google Scholar 

  28. Nishio, T., Kusaba, M., Sakamoto, K. & Ockendon, D. Polymorphism of the kinase domain of the S-locus receptor kinase gene (SRK) in Brassica oleracea L. Theor. Appl. Genet. 95, 335–342 (1997).

    Article  CAS  Google Scholar 

  29. Brace, J., Ockendon, D. J. & King, G. J. Development of a method for identification of S alleles in Brassica oleracea based on digestion of PCR-amplified DNA with restriction endonucleases. Sex. Plant Reprod. 6, 133–138 (1993).

    Article  Google Scholar 

  30. Shiba, H., Hinata, K., Suzuki, A. & Isogai, A. Breakdown of self-incompatibility in Brassica by the antisense RNA of the SLG gene. Proc. Jpn. Acad. B 71, 81–83 (1995).

    Article  Google Scholar 

Download references

Acknowledgements

We thank T.-h. Kao for his critical review and editing of the manuscript. This work was supported in part by Grants-in-Aid for Special research on Priority Areas from the Ministry of Education, Science, Culture and Sports, Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takeshi Takasaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takasaki, T., Hatakeyama, K., Suzuki, G. et al. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403, 913–916 (2000). https://doi.org/10.1038/35002628

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35002628

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

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