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A complex dominance hierarchy is controlled by polymorphism of small RNAs and their targets

Nature Plants volume 3, Article number: 16206 (2017) Cite this article

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Abstract

In diploid organisms, phenotypic traits are often biased by effects known as Mendelian dominant–recessive interactions between inherited alleles. Phenotypic expression of SP11 alleles, which encodes the male determinants of self-incompatibility in Brassica rapa, is governed by a complex dominance hierarchy1–3. Here, we show that a single polymorphic 24 nucleotide small RNA, named SP11 methylation inducer 2 (Smi2), controls the linear dominance hierarchy of the four SP11 alleles (S44 > S60 > S40 > S29). In all dominant–recessive interactions, small RNA variants derived from the linked region of dominant SP11 alleles exhibited high sequence similarity to the promoter regions of recessive SP11 alleles and acted in trans to epigenetically silence their expression. Together with our previous study4, we propose a new model: sequence similarity between polymorphic small RNAs and their target regulates mono-allelic gene expression, which explains the entire five-phased linear dominance hierarchy of the SP11 phenotypic expression in Brassica.

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Figure 1: Identification of Smi2 sequences.
Figure 2: Sequence similarity between Smi2 (sRNA) and the SP11 promoter (target).
Figure 3: Functional analyses of the S60-SMI2 transgene.
Figure 4: ‘Polymorphic dominance modifier’ model for controlling the linear dominance hierarchy with small RNA.

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References

  1. 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 

  2. Shiba, H. et al. The dominance of alleles controlling self- incompatibility in Brassica pollen is regulated at the RNA level. Plant Cell 14, 491–504 (2002).

    Article  CAS  Google Scholar 

  3. Kakizaki, T. et al. Linear dominance relationship among four class-II S haplotypes in pollen is determined by the expression of SP11 in Brassica self-incompatibility. Plant Cell Physiol. 44, 70–75 (2003).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Fisher, R. A. The possible modification of the response of the wild type to recurrent mutations. Am. Nat. 62, 115–126 (1928).

    Article  Google Scholar 

  6. Billiard, S. & Castric, V. Evidence for Fisher's dominance theory: how many ‘special cases’? Trends Genet. 27, 441–445 (2011).

    Article  CAS  Google Scholar 

  7. Takayama, S. & Isogai, A. Self-incompatibility in plants. Annu. Rev. Plant. Biol. 56, 467–489 (2005).

    Article  CAS  Google Scholar 

  8. Suzuki, G. et al. Genomic organization of the S locus: identification and characterization of genes in SLG/SRK region of S(9) haplotype of Brassica campestris (syn. rapa). Genetics 153, 391–400 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 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 

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

    Article  CAS  Google Scholar 

  11. 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  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Kachroo, A., Schopfer, C. R., Nasrallah, M. E. & Nasrallah, J. B. Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 293, 1824–1826 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. Fukai, E., Fujimoto, R. & Nishio, T. Genomic organization of the S core region and the S flanking regions of a class-II S haplotype in Brassica rapa. Mol. Genet. Genomics 269, 361–369 (2003).

    Article  CAS  Google Scholar 

  17. Kakizaki, T. et al. Comparative analysis of the S-intergenic region in class-II S haplotypes of self-incompatible Brassica rapa (syn. campestris). Genes Genet. Syst. 81, 63–67 (2006).

    Article  CAS  Google Scholar 

  18. Shiba, H. et al. Genomic organization of the S-locus region of Brassica. Biosci. Biotechnol. Biochem. 67, 622–626 (2003).

    Article  CAS  Google Scholar 

  19. Kimura, R., Sato, K., Fujimoto, R. & Nishio, T. Recognition specificity of self-incompatibility maintained after the divergence of Brassica oleracea and Brassica rapa. Plant J. 29, 215–223 (2002).

    Article  CAS  Google Scholar 

  20. Chen, C. et al. Real-time quantification of microRNAs by stem-loop RT–PCR. Nucleic Acids Res. 33, e179 (2005).

    Article  Google Scholar 

  21. Bologna, N. G., Mateos, J. L., Bresso, E. G. & Palatnik, J. F. A loop-to-base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159. EMBO J. 28, 3646–3656 (2009).

    Article  CAS  Google Scholar 

  22. Mateos, J. L., Bologna, N. G., Chorostecki, U. & Palatnik, J. F. Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Curr. Biol. 20, 49–54 (2010).

    Article  CAS  Google Scholar 

  23. Zhu, H. et al. Bidirectional processing of pri-miRNAs with branched terminal loops by Arabidopsis Dicer-like1. Nat. Struct. Mol. Biol. 20, 1106–1115 (2013).

    Article  CAS  Google Scholar 

  24. Fahlgren, N. & Carrington, J. C. miRNA target prediction in plants. Methods Mol. Biol. 592, 51–57 (2010).

    Article  CAS  Google Scholar 

  25. Durand, E. et al. Dominance hierarchy arising from the evolution of a complex small RNA regulatory network. Science 346, 1200–1205 (2014).

    Article  CAS  Google Scholar 

  26. Kowyama, Y. et al. Number, frequency and dominance relationships of S-alleles in diploid Ipomoea trifida. Heredity 73, 275–283 (1994).

    Article  Google Scholar 

  27. Brennan, A. C., Tabah, D. A., Harris, S. A. & Hiscock, S. J. Sporophytic self-incompatibility in Senecio squalidus (Asteraceae): S allele dominance interactions and modifiers of cross-compatibility and selfing rates. Heredity 106, 113–123 (2011).

    Article  CAS  Google Scholar 

  28. Casci, T. Gene expression: small but dominant RNA. Nat. Rev. Genet. 11, 670–671 (2010).

    CAS  PubMed  Google Scholar 

  29. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).

    Article  Google Scholar 

Download references

Acknowledgements

We thank K. Kubo for helpful comments and E. Mori, Y. Yamamoto, Y. Yoshimura, F. Kodama, H. Ichikawa, M. Okamura and M. Nara for technical assistance. This work was supported in part by Grants-in-Aid for Scientific Research on Innovative Areas (23113002 and 16H06467 to S.T.; 23113001 to G.S., M.W. and S.T.; 16K21727 and 16H06470 to M.W.; and 16H06464 to M.W. and S.T.) and Grants-in-Aid for Scientific Research (25252021 and 16H06380 to S.T. and 16H04854 to M.W.) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT); the Program for Promotion of Basic Research Activities for Innovative Biosciences (to S.T.) from the Bio-oriented Technology Research Advancement Institution (BRAIN); and Grants in Aid for JSPS Research Fellow (14J10324 to S.Y.) from the Japan Society for the Promotion of Science (JSPS).

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Author notes

  1. Yoshiaki Tarutani & Hiroshi Shiba

    Present address: †Present address: Department of Integrated Genetics, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan (Y.T.); Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan (H.S.),

  2. Shinsuke Yasuda, Yuko Wada and Tomohiro Kakizaki: These authors contributed equally to this work.

Authors and Affiliations

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

    Shinsuke Yasuda, Yuko Wada, Yoshiaki Tarutani, Eiko Miura-Uno, Kohji Murase, Sota Fujii, Tomoya Hioki, Taiki Shimoda, Hiroshi Shiba & Seiji Takayama

  2. Division of Vegetable Breeding, Institute of Vegetable and Floriculture Science, NARO, Tsu, 514-2392, Mie, Japan

    Tomohiro Kakizaki

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

    Yoshinobu Takada & Masao Watanabe

  4. Graduate School of Agricultural Science, Kobe University, Kobe, 657-8501, Hyogo, Japan

    Takeshi Takasaki-Yasuda

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

    Go Suzuki

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

    Seiji Takayama

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Contributions

S.T. and M.W. designed this project. T.K., G.S. and M.W. identified SMI2. S.Y., T.K., G.S., Y. Takada, Y. Tarutani, E.M.-U. and H.S. performed the sequence analyses of the S-locus. S.Y., Y. Tarutani, E.M.-U. and K.M. performed the expression analysis of Smi2. Y.W., E.M.-U., T.H., T.S., Y. Takada, H.S. and T.T.-Y. performed transformation and analysis of transformants. S.F. performed the phylogenetic analysis. S.Y., Y.W. and S.T. wrote the manuscript, which was edited by all of the authors.

Corresponding authors

Correspondence to Masao Watanabe or Seiji Takayama.

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The authors declare no competing financial interests.

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Supplementary Information

Supplementary Methods, Supplementary Figures 1–5, Supplementary Tables 1–5, Supplementary References. (PDF 1008 kb)

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Yasuda, S., Wada, Y., Kakizaki, T. et al. A complex dominance hierarchy is controlled by polymorphism of small RNAs and their targets. Nature Plants 3, 16206 (2017). https://doi.org/10.1038/nplants.2016.206

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