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Direct ligand–receptor complex interaction controls Brassica self-incompatibility

Nature volume 413, pages 534–538 (2001)Cite this article

Abstract

Many higher plants have evolved self-incompatibility mechanisms to prevent self-fertilization1. In Brassica self-incompatibility, recognition between pollen and the stigma is controlled by the S locus, which contains three highly polymorphic genes: S-receptor kinase (SRK)2, S-locus protein 11 (SP11)3 (also called S-locus cysteine-rich protein; SCR)4 and S-locus glycoprotein (SLG)5. SRK encodes a membrane-spanning serine/threonine kinase that determines the S-haplotype specificity of the stigma6, and SP11 encodes a small cysteine-rich protein that determines the S-haplotype specificity of pollen4,7,8. SP11 is localized in the pollen coat8. It is thought that, during self-pollination, SP11 is secreted from the pollen coat and interacts with its cognate SRK in the papilla cell of the stigma to elicit the self-incompatibility response. SLG is a secreted stigma protein9 that is highly homologous to the SRK extracellular domain. Although it is not required for S-haplotype specificity of the stigma, SLG enhances the self-incompatibility response6; however, how this is accomplished remains controversial10,11,12. Here we show that a single form of SP11 of the S8 haplotype (S8-SP11) stabilized with four intramolecular disulphide bonds specifically binds the stigma membrane of the S8 haplotype to induce autophosphorylation of SRK8, and that SRK8 and SLG8 together form a high-affinity receptor complex for S8-SP11 on the stigma membrane.

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Figure 1: Molecular characterization of S8-SP11.
Figure 2: Surface plasmon resonance measurement of the affinity of SP11s for SLGs and a recombinant SRK extracellular domain.
Figure 3: Specific 125I-labelled S8-SP11 binding to microsomal membranes of the stigma.
Figure 4: Interaction of S8-SP11 with SRK8–SLG8 receptor complex.

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References

  1. McCubbin, A. G. & Kao, T.-h. Molecular recognition and response in pollen and pistil interactions. Annu. Rev. Cell Dev. Biol. 16, 333–364 (2000).

    Article  CAS  Google Scholar 

  2. Stein, J. C., Howlett, B., Boyes, D. C., Nasrallah, M. E. & Nasrallah, J. B. 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. 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 

  4. 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 

  5. 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 

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

    Article  ADS  CAS  Google Scholar 

  7. Takayama, S. et al. The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl Acad. Sci. USA 97, 1920–1925 (2000).

    Article  ADS  CAS  Google Scholar 

  8. Shiba, H. et al. A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol. 125, 2095–2103 (2001).

    Article  CAS  Google Scholar 

  9. Takayama, S. et al. Sequences of S-glycoproteins, products of the Brassica campestris self-incompatibility locus. Nature 326, 102–104 (1987).

    Article  ADS  CAS  Google Scholar 

  10. Torii, K. U. Receptor kinase activation and signal transduction in plants: an emerging picture. Curr. Opin. Plant Biol. 3, 361–367 (2000).

    Article  CAS  Google Scholar 

  11. Dickinson, H. G. Pollen stigma interactions: so near yet so far. Trends Genet. 16, 373–376 (2000).

    Article  CAS  Google Scholar 

  12. Brugière, N., Cui, Y. & Rothstein, S. J. Molecular mechanisms of self-recognition in Brassica self-incompatibility. Trends Plant Sci. 5, 432–438 (2000).

    Article  Google Scholar 

  13. Broekaert, W. F., Terras, F. R. G., Cammue, B. P. A. & Osborn, R. W. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol. 108, 1353–1358 (1995).

    Article  CAS  Google Scholar 

  14. Bruix, M. et al. Solution structure of γ1-H and γ1-P thionins from barley and wheat endosperm determined by 1H-NMR: A structural motif common to toxic arthropod proteins. Biochemistry 32, 715–724 (1993).

    Article  CAS  Google Scholar 

  15. Watanabe, M. et al. Highly divergent sequences of the pollen self-incompatibility (S) gene in class-I S haplotypes of Brassica campestris (syn. rapa) L. FEBS Lett. 473, 139–144 (2000).

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

    Article  CAS  Google Scholar 

  17. Doughty, J. et al. PCP-A1, a defensin-like Brassica pollen coat protein that binds the S locus glycoprotein, is the product of gametophytic gene expression. Plant Cell 10, 1333–1347 (1998).

    Article  CAS  Google Scholar 

  18. Takayama, S. et al. Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollen-stigma adhesion. Proc. Natl Acad. Sci. USA 97, 3765–3770 (2000).

    Article  ADS  CAS  Google Scholar 

  19. Trotochaud, A. E., Jeong, S. & Clark, S. E. CLAVATA3, a multimeric ligand for the CLAVATA1 receptor-kinase. Science 289, 613–617 (2000).

    Article  ADS  CAS  Google Scholar 

  20. Gómez-Gómez, L., Bauer, Z. & Boller, T. Both the extracellular leucine-rich repeat domain and the kinase activity of FLS2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13, 1155–1163 (2001).

    Article  Google Scholar 

  21. Wang, Z.-Y., Seto, H., Fujioka, S., Yoshida, S. & Chory, J. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410, 380–383 (2001).

    Article  ADS  CAS  Google Scholar 

  22. 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 SRK extracellular domain in Brassica oleracea. Plant J. 8, 827–834 (1995).

    Article  CAS  Google Scholar 

  23. Suzuki, G., Watanabe, M., Toriyama, K., Isogai, A. & Hinata, K. Expression of SLG 9 and SRK 9 genes in transgenic tobacco. Plant Cell Physiol. 37, 866–869 (1996).

    Article  CAS  Google Scholar 

  24. 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 

  25. Dixit, R., Nasrallah, M. E. & Nasrallah, J. B. Post-transcriptional maturation of the S receptor kinase of Brassica correlates with co-expression of the S-locus glycoprotein in the stigmas of two Brassica strains and in transgenic tobacco plants. Plant Physiol. 124, 297–311 (2000).

    Article  CAS  Google Scholar 

  26. Suzuki, T., Kusaba, M., Matsushita, M., Okazaki, K. & Nishio, T. Characterization of Brassica S-haplotypes lacking S-locus glycoprotein. FEBS Lett. 482, 102–108 (2000).

    Article  CAS  Google Scholar 

  27. Cabrillac, D., Cock, J. M., Dumas, C. & Gaude, T. The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins. Nature 410, 220–223 (2001).

    Article  ADS  CAS  Google Scholar 

  28. Kojima, M. et al. Ghrelin is a growth-hormone-releasing acylated peptide form stomach. Nature 402, 656–660 (1999).

    Article  ADS  CAS  Google Scholar 

  29. Shiba, H. et al. Alteration of the self-incompatibility phenotype in Brassica by transformation of the antisense SLG gene. Biosci. Biotechnol. Biochem. 64, 1016–1024 (2000).

    Article  CAS  Google Scholar 

  30. Larsson, C., Widell, S. & Kjellbom, P. Preparation of high-purity plasma membranes. Methods Enzymol. 148, 558–568 (1987).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank T.-H. Kao for critically reading and editing the manuscript; and H. Sugita, T. Ueda, K. Iwasaki and H. Sato for technical assistance. This work was supported in part by grants-in-aid from the Ministry of Education, Culture, Sports, Science and Technology, and grants from The Japan Society for the Promotion of Science.

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  1. Seiji Takayama, Hiroko Shimosato and Masao Watanabe: These authors contributed equally to this work

Authors and Affiliations

  1. Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, 630-0101, Japan

    Seiji Takayama, Hiroko Shimosato, Hiroshi Shiba, Miyuki Funato, Fang-Sik Che, Megumi Iwano & Akira Isogai

  2. Faculty of Agriculture, Iwate University, 3-18-8 Ueda, Morioka, 020-8550, Japan

    Masao Watanabe

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Correspondence to Akira Isogai.

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Takayama, S., Shimosato, H., Shiba, H. et al. Direct ligand–receptor complex interaction controls Brassica self-incompatibility. Nature 413, 534–538 (2001). https://doi.org/10.1038/35097104

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