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Dominance in self-compatibility between subgenomes of allopolyploid Arabidopsis kamchatica shown by transgenic restoration of self-incompatibility

Author

Listed:
  • Chow-Lih Yew

    (University of Zurich
    University of Zurich)

  • Takashi Tsuchimatsu

    (University of Zurich
    University of Zurich
    University of Tokyo)

  • Rie Shimizu-Inatsugi

    (University of Zurich
    University of Zurich)

  • Shinsuke Yasuda

    (Nara Institute of Science and Technology)

  • Masaomi Hatakeyama

    (University of Zurich
    University of Zurich
    Functional Genomics Center Zurich)

  • Hiroyuki Kakui

    (University of Zurich
    Yokohama City University
    University of Tokyo
    Kyoto University)

  • Takuma Ohta

    (Mie University)

  • Keita Suwabe

    (Mie University)

  • Masao Watanabe

    (Tohoku University)

  • Seiji Takayama

    (Nara Institute of Science and Technology
    University of Tokyo)

  • Kentaro K. Shimizu

    (University of Zurich
    University of Zurich
    Yokohama City University)

Abstract

The evolutionary transition to self-compatibility facilitates polyploid speciation. In Arabidopsis relatives, the self-incompatibility system is characterized by epigenetic dominance modifiers, among which small RNAs suppress the expression of a recessive SCR/SP11 haplogroup. Although the contribution of dominance to polyploid self-compatibility is speculated, little functional evidence has been reported. Here we employ transgenic techniques to the allotetraploid plant A. kamchatica. We find that when the dominant SCR-B is repaired by removing a transposable element insertion, self-incompatibility is restored. This suggests that SCR was responsible for the evolution of self-compatibility. By contrast, the reconstruction of recessive SCR-D cannot restore self-incompatibility. These data indicate that the insertion in SCR-B conferred dominant self-compatibility to A. kamchatica. Dominant self-compatibility supports the prediction that dominant mutations increasing selfing rate can pass through Haldane’s sieve against recessive mutations. The dominance regulation between subgenomes inherited from progenitors contrasts with previous studies on novel epigenetic mutations at polyploidization termed genome shock.

Suggested Citation

  • Chow-Lih Yew & Takashi Tsuchimatsu & Rie Shimizu-Inatsugi & Shinsuke Yasuda & Masaomi Hatakeyama & Hiroyuki Kakui & Takuma Ohta & Keita Suwabe & Masao Watanabe & Seiji Takayama & Kentaro K. Shimizu, 2023. "Dominance in self-compatibility between subgenomes of allopolyploid Arabidopsis kamchatica shown by transgenic restoration of self-incompatibility," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43275-2
    DOI: 10.1038/s41467-023-43275-2
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    as
    1. Takashi Tsuchimatsu & Keita Suwabe & Rie Shimizu-Inatsugi & Sachiyo Isokawa & Pavlos Pavlidis & Thomas Städler & Go Suzuki & Seiji Takayama & Masao Watanabe & Kentaro K. Shimizu, 2010. "Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene," Nature, Nature, vol. 464(7293), pages 1342-1346, April.
    2. Yoshiaki Tarutani & Hiroshi Shiba & Megumi Iwano & Tomohiro Kakizaki & Go Suzuki & Masao Watanabe & Akira Isogai & Seiji Takayama, 2010. "Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility," Nature, Nature, vol. 466(7309), pages 983-986, August.
    3. Timothy Paape & Roman V. Briskine & Gwyneth Halstead-Nussloch & Heidi E. L. Lischer & Rie Shimizu-Inatsugi & Masaomi Hatakeyama & Kenta Tanaka & Tomoaki Nishiyama & Renat Sabirov & Jun Sese & Kentaro , 2018. "Patterns of polymorphism and selection in the subgenomes of the allopolyploid Arabidopsis kamchatica," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    4. Sean P. Gordon & Bruno Contreras-Moreira & Joshua J. Levy & Armin Djamei & Angelika Czedik-Eysenberg & Virginia S. Tartaglio & Adam Session & Joel Martin & Amy Cartwright & Andrew Katz & Vasanth R. Si, 2020. "Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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