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.

Duplicated pollen–pistil recognition loci control intraspecific unilateral incompatibility in Brassica rapa

Abstract

In plants, cell–cell recognition is a crucial step in the selection of optimal pairs of gametes to achieve successful propagation of progeny. Flowering plants have evolved various genetic mechanisms, mediated by cell–cell recognition, to enable their pistils to reject self-pollen, thus preventing inbreeding and the consequent reduced fitness of progeny (self-incompatibility, SI), and to reject foreign pollen from other species, thus maintaining species identity (interspecific incompatibility)1. In the genus Brassica, the SI system is regulated by an S-haplotype-specific interaction between a stigma-expressed female receptor (S receptor kinase, SRK) and a tapetum cell-expressed male ligand (S locus protein 11, SP11), encoded by their respective polymorphic genes at the S locus26. However, the molecular mechanism for recognition of foreign pollen, leading to reproductive incompatibility, has not yet been identified. Here, we show that recognition between a novel pair of proteins, a pistil receptor SUI1 (STIGMATIC UNILATERAL INCOMPATIBILITY 1) and a pollen ligand PUI1 (POLLEN UNILATERAL INCOMPATIBILITY 1), triggers unilateral reproductive incompatibility between plants of two geographically distant self-incompatible Brassica rapa lines, even though crosses would be predicted to be compatible based on the S haplotypes of pollen and stigma. Interestingly, SUI1 and PUI1 are similar to the SI genes, SRK and SP11, respectively, and are maintained as cryptic incompatibility genes in these two populations. The duplication of the SRK and SP11 followed by reciprocal loss in different populations would provide a molecular mechanism of the emergence of a reproductive barrier in allopatry.

Your institute does not have access to this article

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Map-based cloning of candidate genes for SUI and PUI.
Figure 2: Functional complementation of SUI1.
Figure 3: Functional complementation of PUI1.
Figure 4: Lack of SUI1PUI1 orthologues in Arabidopsis and phylogeny of SUI1.

References

  1. de Nettancourt, D. Incompatibility and Incongruity in Wild and Cultivated Plants (Springer, 2001).

    Book  Google Scholar 

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

    CAS  Article  PubMed  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 Central  PubMed  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).

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Takayama, S. et al. Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413, 534–538 (2001).

    CAS  Article  PubMed  Google Scholar 

  7. Lewis, D. & Crowe, L. K. Unilateral interspecific incompatibility in flowering plants. Heredity 12, 233–256 (1958).

    Article  Google Scholar 

  8. Hiscock, S. J. & Dickinson, H. G. Unilateral incompatibility within the Brassicaceae: further evidence for the involvement of the self-incompatibility (S)-locus. Theor. Appl. Genet. 86, 744–753 (1993).

    CAS  Article  PubMed  Google Scholar 

  9. Murfett, J. et al. S RNase and interspecific pollen rejection in the genus Nicotiana: multiple pollen-rejection pathways contribute to unilateral incompatibility between self-incompatible and self-compatible species. Plant Cell 8, 943–958 (1996).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Hancock, C. N., Kondo, K., Beecher, B. & McClure, B. The S-locus and unilateral incompatibility. Phil. Trans. R. Soc. Lond. B 358, 1133–1140 (2003).

    CAS  Article  Google Scholar 

  11. Li, W. & Chetelat, R. T. A pollen factor linking inter- and intraspecific pollen rejection in tomato. Science 330, 1827–1830 (2010).

    CAS  Article  PubMed  Google Scholar 

  12. Li, W. & Chetelat, R. T. The role of a pollen-expressed Cullin1 protein in gametophytic self-incompatibility in Solanum. Genetics 196, 439–442 (2014).

    CAS  Article  PubMed  Google Scholar 

  13. Li, W. & Chetelat, R. T. Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species. Proc. Natl Acad. Sci. USA 112, 4417–4422 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Kubo, K. et al. Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science 330, 796–799 (2010).

    CAS  Article  PubMed  Google Scholar 

  15. Williams, J. S., Der, J. P., dePamphilis, C. W. & Kao, T.-h. Transcriptome analysis reveals the same 17 S-locus F-box genes in two haplotypes of the self-incompatibility locus of Petunia inflata. Plant Cell 26, 2873–2888 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Kubo, K. et al. Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia. Nat. Plants 1, 14005 (2015).

    CAS  Article  PubMed  Google Scholar 

  17. Udagawa, H. et al. Genetic analysis of interspecific incompatibility in Brassica rapa. Theor. Appl. Genet. 121, 689–696 (2010).

    CAS  Article  PubMed  Google Scholar 

  18. Takada, Y. et al. Genetic analysis of novel intra-species unilateral incompatibility in Brassica rapa (syn. campestris) L. Sex. Plant Reprod. 17, 211–217 (2005).

    Article  Google Scholar 

  19. Takada, Y. et al. Involvement of MLPK pathway in intraspecies unilateral incompatibility regulated by a single locus with stigma and pollen factors. Genes Genomes Genet. 3, 719–726 (2013).

    CAS  Google Scholar 

  20. Murase, K. et al. A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303, 1516–1519 (2004).

    CAS  Article  PubMed  Google Scholar 

  21. Kakita, M. et al. Two distinct forms of M-locus protein kinase localize to the plasma membrane and interact directly with S-locus receptor kinase to transduce self-incompatibility signaling in Brassica rapa. Plant Cell 19, 3961–3973 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Kai, N., Suzuki, G., Watanabe, M., Isogai, A. & Hinata, K. Sequence comparisons among dispersed members of the Brassica S multigene family in an S9 genome. Mol. Genet. Genomics 265, 526–534 (2001).

    CAS  Article  PubMed  Google Scholar 

  23. Shimosato, H. et al. Characterization of the SP11/SCR high-affinity biding site involved in self/nonself recognition in Brassica self-incompatibility. Plant Cell 19, 107–117 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Cock, J. M., Stanchev, B., Delorme, V., Croy, R. R. D. & Dumas, C. SLR3: a modified receptor kinase gene that has been adapted to encode a putative secreted glycoprotein similar to the S locus glycoprotein. Mol. Gen. Genet. 248, 151–161 (1995).

    CAS  Article  PubMed  Google Scholar 

  25. Zhang, X., Wang, L., Yuan, Y., Tian, D. & Yang, S. Rapid copy number expansion and recent recruitment of domains in S-receptor kinase-like genes contribute to the origin of self-incompatibility. FEBS J. 278, 4323–4337 (2011).

    CAS  Article  PubMed  Google Scholar 

  26. Dereeper, A. et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465–W469 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Chantha, S.-C., Herman, A. C., Platts, A. E., Vekemans, X. & Schoen, D. J. Secondary evolution of a self-incompatibility locus in the Brassicaceae genus Leavenworthia. PLoS Biol. 11, e1001560 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Shimizu, K. K. & Tsuchimatsu, T. Evolution of selfing: recurrent patterns in molecular adaptation. Annu. Rev. Ecol. Syst. 46, 593–622 (2015).

    Article  Google Scholar 

  29. Tsuchimatsu, T. et al. Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 464, 1342–1346 (2010).

    CAS  Article  PubMed  Google Scholar 

  30. Kitashiba, H. & Nasrallah, J. B. Self-incompatibility in Brassicaceae crops: lessons for interspecific incompatibility. Breed. Sci. 64, 23–37 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 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 

  32. Nou, I. S., Watanabe, M., Isogai, A. & Hinata, K. Comparison of S-alleles and S-glycoproteins between two wild populations of Brassica campestris in Turkey and Japan. Sex. Plant Reprod. 6, 79–86 (1993).

    Article  Google Scholar 

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

    Google Scholar 

  34. Suwabe, K. et al. Simple sequence repeat-based comparative genomics between Brassica rapa and Arabidopsis thaliana: the genetic origin of clubroot resistance. Genetics 173, 309–319 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Wang, X. et al. The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43, 1035–1039 (2011).

    CAS  Article  PubMed  Google Scholar 

  36. Murray, M. G. & Thompson, W. F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8, 4321–4325 (1980).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Shiba, H. et al. Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nat. Genet. 38, 297–299 (2006).

    CAS  Article  PubMed  Google Scholar 

  38. Tarutani, Y. et al. Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature 466, 983–986 (2010).

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank K. Ito, H. Masuko-Suzuki, Y. Sasajima, K. Takemoto, M. Hiraiwa, M. Takeda and M. Uchino for technical assistance. This work was supported in part by MEXT KAKENHI grant numbers 23113006 to G.S.;16H06469 and 26113709 to K.K.S.; 23113001, 23113002 and 16H06467 to S.T.; 26300003, 16H06470, 16H06464 and 16K21727 to M.W. and JSPS KAKENHI grant numbers 16H05066 to K.S.; 16H06380 to S.T.; 25252001, 16H04854 and 16K15085 to M.W.; 26850001 and 17K15208 to Y.T. and by Golden Seed Project (no. 213006-05-1-SB110), MAFRA, MOF, RDA, KFS, Republic of Korea to Y.P.L.; Swiss National Foundation to K.K.S. This research was also supported by Japan Advanced Plant Science Network to M.W.

Author information

Authors and Affiliations

Authors

Contributions

Y.T., G.S., K.K.S., S.T. and M.W. conceived and designed the experiments. Y.T., K.M., Y.S.-A., T.S. and H.N. performed the research and analysed the data. T.S., K.S. and Y.P.L. contributed to the positional cloning of SUI1 and PUI1. Y.T., G.S. and M.W. wrote the paper, which was edited by all other authors.

Corresponding authors

Correspondence to Go Suzuki or Masao Watanabe.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–11, Supplementary Tables 1–4. (PDF 14856 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Takada, Y., Murase, K., Shimosato-Asano, H. et al. Duplicated pollen–pistil recognition loci control intraspecific unilateral incompatibility in Brassica rapa. Nature Plants 3, 17096 (2017). https://doi.org/10.1038/nplants.2017.96

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2017.96

Further reading

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