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Genomic structural variation-mediated allelic suppression causes hybrid male sterility in rice

Author

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  • Rongxin Shen

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Lan Wang

    (Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Xupeng Liu

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Jiang Wu

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Weiwei Jin

    (National Maize Improvement Center of China, Key Laboratory of Crop Genetic Improvement and Genome of Ministry of Agriculture, Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University)

  • Xiucai Zhao

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Xianrong Xie

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Qinlong Zhu

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Huiwu Tang

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Qing Li

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Letian Chen

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

  • Yao-Guang Liu

    (State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources
    Key Laboratory of Plant Functional Genomics and Biotechnology of Guangdong Provincial Higher Education Institutions
    College of Life Sciences, South China Agricultural University)

Abstract

Hybrids between divergent populations commonly show hybrid sterility; this reproductive barrier hinders hybrid breeding of the japonica and indica rice (Oryza sativa L.) subspecies. Here we show that structural changes and copy number variation at the Sc locus confer japonica–indica hybrid male sterility. The japonica allele, Sc-j, contains a pollen-essential gene encoding a DUF1618-domain protein; the indica allele, Sc-i, contains two or three tandem-duplicated ~ 28-kb segments, each carrying an Sc-j-homolog with a distinct promoter. In Sc-j/Sc-i hybrids, the high-expression of Sc-i in sporophytic cells causes suppression of Sc-j expression in pollen and selective abortion of Sc-j-pollen, leading to transmission ratio distortion. Knocking out one or two of the three Sc-i copies by CRISPR/Cas9 rescues Sc-j expression and male fertility. Our results reveal the gene dosage-dependent allelic suppression as a mechanism of hybrid incompatibility, and provide an effective approach to overcome the reproductive barrier for hybrid breeding.

Suggested Citation

  • Rongxin Shen & Lan Wang & Xupeng Liu & Jiang Wu & Weiwei Jin & Xiucai Zhao & Xianrong Xie & Qinlong Zhu & Huiwu Tang & Qing Li & Letian Chen & Yao-Guang Liu, 2017. "Genomic structural variation-mediated allelic suppression causes hybrid male sterility in rice," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-01400-y
    DOI: 10.1038/s41467-017-01400-y
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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. 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.
    3. 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.
    4. Jingfen Huang & Yilin Zhang & Yapeng Li & Meng Xing & Cailin Lei & Shizhuang Wang & Yamin Nie & Yanyan Wang & Mingchao Zhao & Zhenyun Han & Xianjun Sun & Han Zhou & Yan Wang & Xiaoming Zheng & Xiaoron, 2024. "Haplotype-resolved gapless genome and chromosome segment substitution lines facilitate gene identification in wild rice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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