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

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 hierarchy13. 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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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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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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