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

Nature Plants volume 3, Article number: 17096 (2017) Cite this article

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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 locus2–6. 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.

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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 SUI1–PUI1 orthologues in Arabidopsis and phylogeny of SUI1.

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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.

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Authors and Affiliations

  1. Graduate School of Life Sciences, Tohoku University, 980-8577, Sendai, Japan

    Yoshinobu Takada, Takahiro Sato & Masao Watanabe

  2. Graduate School of Biological Sciences, Nara Institute of Science and Technology, 630-0192, Ikoma, Japan

    Kohji Murase, Hiroko Shimosato-Asano & Seiji Takayama

  3. Department of Applied Biological Chemistry, The University of Tokyo, 113-8657, Tokyo, Japan

    Kohji Murase & Seiji Takayama

  4. Division of Natural Science, Osaka Kyoiku University, 582-8582, Kashiwara, Japan

    Honoka Nakanishi & Go Suzuki

  5. Graduate School of Bioresources, Mie University, 514-8507, Tsu, Japan

    Keita Suwabe

  6. Department of Evolutionary Biology and Environmental Studies, University of Zurich, CH-8057, Zurich, Switzerland

    Kentaro K. Shimizu

  7. Kihara Institute for Biological Research, Yokohama City University, 244-0813, Yokohama, Japan

    Kentaro K. Shimizu

  8. Department of Horticulture, Chungnam National University, 34134, Daejeon, Korea

    Yong Pyo Lim

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  1. Yoshinobu Takada
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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.

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Correspondence to Go Suzuki or Masao Watanabe.

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The authors declare no competing financial interests.

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Supplementary Information

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

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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

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