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Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

Nature Plants volume 1, Article number: 14005 (2015) Cite this article

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Abstract

Self-incompatibility (SI) systems in flowering plants distinguish self- and non-self pollen to prevent inbreeding. While other SI systems rely on the self-recognition between specific male- and female-determinants, the Solanaceae family has a non-self recognition system resulting in the detoxification of female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen. It is not known how many SLF components of this non-self recognition system there are in Solanaceae species, or how they evolved. We identified 16–20 SLFs in each S-haplotype in SI Petunia, from a total of 168 SLF sequences using large-scale next-generation sequencing and genomic polymerase chain reaction (PCR) techniques. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated these predictions by transformation experiments. A simple mathematical model confirmed that 16–20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to the constitution of a non-self recognition system and also contribute to self-compatible mutations.

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Figure 1: Phylogenies of SLFs and S-RNases from Petunia.
Figure 2: Relationships between phylogenies of SLFs and SLF/S-RNase interactions.
Figure 3: Target S-RNase analysis of S5-SLF3.
Figure 4: Phylogenies and pericentromeric localization of Solanaceae SLFs and S-RNases.
Figure 5: Estimation of the proportion of S-RNase recognized by multiple SLF types.
Figure 6: Model for the evolution of SLFs.

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Acknowledgements

We thank H. Takatsuji at the National Institute of Agrobiological Sciences for P. hybrida cv. Mitchell and W138; S. Saha at Cornel University for directions on Solanum genomic information; M. Iwano, H. Shiba, H. Shimosato-Asano, Y. Wada, K. Murase, M. Kakita, E. Miura, H. Kakui, T. Tsuchimatsu and M. Robinson for discussion or technical advice; and F. Kodama, M. Okamura, E. Mori, Y. Goto, H. Kikuchi, and Functional Genomics Centre Zurich for technical assistance. We thank T-h. Kao at Pennsylvania State University for adapting a unified nomenclature for the same new SLF genes before publication. This work was supported in part by a Grant-in-Aid for Scientific Research on Innovative Areas (23113002) and by Grants-in-Aid for Scientific Research (21248014, 25252021) from the Ministry of Education, Culture, Sports, Science and Technology of Japan awarded to S.T. This work was also supported in part by Swiss National Science Foundation (31003A_140917) and by URPP Evolution in Action of University of Zurich awarded to K.K.S., Marie-Heim Vögtlin grant awarded to R.S-I. and by Plant Fellows awarded to T.P.

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Authors and Affiliations

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

    Ken-ichi Kubo, Tetsuyuki Entani, Akie Takara, Kie Kajihara, Mai Tsukahara & Seiji Takayama

  2. Institute of Evolutionary Biology and Environmental Studies, University of Zurich, CH-8057 Zurich, Switzerland

    Timothy Paape, Masaomi Hatakeyama, Rie Shimizu-Inatsugi & Kentaro K. Shimizu

  3. Functional Genomics Center Zurich, CH-8057 Zurich, Switzerland

    Masaomi Hatakeyama

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  1. Ken-ichi Kubo
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Contributions

K-i.K., K.K.S. and S.T. planned and designed the research. K-i.K. and T.E. constructed pollen cDNA libraries. M.H. and R.S-I. performed next generation sequencing and construction of pollen EST databases. K-i.K. and K.K. performed isolation and Sanger sequencing of cDNA and genomic clones. K-i.K. and A.T. performed construction and analysis of transgenic plants. K-i.K. and T.P. performed phylogenetic and evolutionary analyses. K-i.K. and M.T. performed linkage analysis and expression profiling. M.H. and K.K.S. designed mathematical models and performed simulations. S.T. initiated and guided the project. K-i.K., T.P., M.H., K.K.S. and S.T. wrote the manuscript.

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Correspondence to Kentaro K. Shimizu or Seiji Takayama.

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Kubo, Ki., Paape, T., Hatakeyama, M. et al. Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia. Nature Plants 1, 14005 (2015). https://doi.org/10.1038/nplants.2014.5

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