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An asymmetric allelic interaction drives allele transmission bias in interspecific rice hybrids

Author

Listed:
  • Yongyao Xie

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Jintao Tang

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Xianrong Xie

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Xiaojuan Li

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Jianle Huang

    (South China Agricultural University
    South China Agricultural University)

  • Yue Fei

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Jingluan Han

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Shuifu Chen

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Huiwu Tang

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Xiucai Zhao

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Dayun Tao

    (Yunnan Academy of Agricultural Sciences)

  • Peng Xu

    (Yunnan Academy of Agricultural Sciences
    Chinese Academy of Sciences)

  • Yao-Guang Liu

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

  • Letian Chen

    (South China Agricultural University
    South China Agricultural University
    South China Agricultural University
    South China Agricultural University)

Abstract

Hybrid sterility (HS) between Oryza sativa (Asian rice) and O. glaberrima (African rice) is mainly controlled by the S1 locus. However, our limited understanding of the HS mechanism hampers utilization of the strong interspecific heterosis. Here, we show that three closely linked genes (S1A4, S1TPR, and S1A6) in the African S1 allele (S1-g) constitute a killer-protector system that eliminates gametes carrying the Asian allele (S1-s). In Asian–African rice hybrids (S1-gS1-s), the S1TPR-S1A4-S1A6 interaction in sporophytic tissues generates an abortion signal to male and female gametes. However, S1TPR can rescue S1-g gametes, while the S1-s gametes selectively abort for lacking S1TPR. Knockout of any of the S1-g genes eliminates the HS. Evolutionary analysis suggests that S1 may have arisen from newly evolved genes, multi-step recombination, and nucleotide variations. Our findings will help to overcome the interspecific reproductive barrier and use Asian–African hybrids for increasing rice production.

Suggested Citation

  • Yongyao Xie & Jintao Tang & Xianrong Xie & Xiaojuan Li & Jianle Huang & Yue Fei & Jingluan Han & Shuifu Chen & Huiwu Tang & Xiucai Zhao & Dayun Tao & Peng Xu & Yao-Guang Liu & Letian Chen, 2019. "An asymmetric allelic interaction drives allele transmission bias in interspecific rice hybrids," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-10488-3
    DOI: 10.1038/s41467-019-10488-3
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    Cited by:

    1. Daiqi Wang & Hongru Wang & Xiaomei Xu & Man Wang & Yahuan Wang & Hong Chen & Fei Ping & Huanhuan Zhong & Zhengkun Mu & Wantong Xie & Xiangyu Li & Jingbin Feng & Milan Zhang & Zhilan Fan & Tifeng Yang , 2023. "Two complementary genes in a presence-absence variation contribute to indica-japonica reproductive isolation in rice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Myint Zin Mar & Yohei Koide & Mei Ogata & Daichi Kuniyoshi & Yoshiki Tokuyama & Kiwamu Hikichi & Mitsuhiro Obara & Yuji Kishima, 2021. "Genetic Mapping of the Gamete Eliminator Locus, S 2 , Causing Hybrid Sterility and Transmission Ratio Distortion Found between Oryza sativa and Oryza glaberrima Cross Combination," Agriculture, MDPI, vol. 11(3), pages 1-10, March.
    3. Shimin You & Zhigang Zhao & Xiaowen Yu & Shanshan Zhu & Jian Wang & Dekun Lei & Jiawu Zhou & Jing Li & Haiyuan Chen & Yanjia Xiao & Weiwei Chen & Qiming Wang & Jiayu Lu & Keyi Chen & Chunlei Zhou & Xi, 2023. "A toxin-antidote system contributes to interspecific reproductive isolation in rice," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Ben Liao & You-Huang Xiang & Yan Li & Kai-Yang Yang & Jun-Xiang Shan & Wang-Wei Ye & Nai-Qian Dong & Yi Kan & Yi-Bing Yang & Huai-Yu Zhao & Hong-Xiao Yu & Zi-Qi Lu & Yan Zhao & Qiang Zhao & Dongling G, 2024. "Dysfunction of duplicated pair rice histone acetyltransferases causes segregation distortion and an interspecific reproductive barrier," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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