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Two complementary genes in a presence-absence variation contribute to indica-japonica reproductive isolation in rice

Author

Listed:
  • Daiqi Wang

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

  • Hongru Wang

    (Chinese Academy of Agricultural Sciences)

  • Xiaomei Xu

    (South China Agricultural University)

  • Man Wang

    (South China Agricultural University
    South China Agricultural University)

  • Yahuan Wang

    (South China Agricultural University)

  • Hong Chen

    (South China Agricultural University)

  • Fei Ping

    (South China Agricultural University
    South China Agricultural University)

  • Huanhuan Zhong

    (South China Agricultural University)

  • Zhengkun Mu

    (South China Agricultural University
    South China Agricultural University)

  • Wantong Xie

    (South China Agricultural University
    South China Agricultural University)

  • Xiangyu Li

    (South China Agricultural University
    South China Agricultural University)

  • Jingbin Feng

    (South China Agricultural University
    South China Agricultural University)

  • Milan Zhang

    (South China Agricultural University
    South China Agricultural University)

  • Zhilan Fan

    (Guangdong Academy of Agricultural Sciences)

  • Tifeng Yang

    (Guangdong Academy of Agricultural Sciences)

  • Junliang Zhao

    (Guangdong Academy of Agricultural Sciences)

  • Bin Liu

    (Guangdong Academy of Agricultural Sciences)

  • Ying Ruan

    (Hunan Agricultural University
    Hunan Agricultural University)

  • Guiquan Zhang

    (South China Agricultural University
    South China Agricultural University)

  • Chunlin Liu

    (Hunan Agricultural University
    Hunan Agricultural University)

  • Ziqiang Liu

    (South China Agricultural University
    South China Agricultural University)

Abstract

Understanding the evolutionary forces in speciation is a central goal in evolutionary biology. Asian cultivated rice has two subspecies, indica and japonica, but the underlying mechanism of the partial reproductive isolation between them remains obscure. Here we show a presence-absence variation (PAV) at the Se locus functions as an indica-japonica reproductive barrier by causing hybrid sterility (HS) in indica-japonica crosses. The locus comprises two adjacent genes: ORF3 encodes a sporophytic pollen killer, whereas ORF4 protects pollen in a gametophytic manner. In F1 of indica-japonica crosses, pollen with the japonica haplotype, which lacks the sequence containing the protective ORF4, is aborted due to the pollen-killing effect of ORF3 from indica. Evolutionary analysis suggests ORF3 is a gene associated with the Asian cultivated rice species complex, and the PAV has contributed to the reproductive isolation between the two subspecies of Asian cultivated rice. Our analyses provide perspectives on rice inter-subspecies post-zygotic isolation, and will promote efforts to overcome reproductive barriers in indica-japonica hybrid rice breeding.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40189-x
    DOI: 10.1038/s41467-023-40189-x
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    as
    1. Hongbo Li & Shenhao Wang & Sen Chai & Zhiquan Yang & Qiqi Zhang & Hongjia Xin & Yuanchao Xu & Shengnan Lin & Xinxiu Chen & Zhiwang Yao & Qingyong Yang & Zhangjun Fei & Sanwen Huang & Zhonghua Zhang, 2022. "Graph-based pan-genome reveals structural and sequence variations related to agronomic traits and domestication in cucumber," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Yoko Hattori & Keisuke Nagai & Shizuka Furukawa & Xian-Jun Song & Ritsuko Kawano & Hitoshi Sakakibara & Jianzhong Wu & Takashi Matsumoto & Atsushi Yoshimura & Hidemi Kitano & Makoto Matsuoka & Hitoshi, 2009. "The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water," Nature, Nature, vol. 460(7258), pages 1026-1030, August.
    3. Wensheng Wang & Ramil Mauleon & Zhiqiang Hu & Dmytro Chebotarov & Shuaishuai Tai & Zhichao Wu & Min Li & Tianqing Zheng & Roven Rommel Fuentes & Fan Zhang & Locedie Mansueto & Dario Copetti & Millicen, 2018. "Genomic variation in 3,010 diverse accessions of Asian cultivated rice," Nature, Nature, vol. 557(7703), pages 43-49, May.
    4. Susan R. McCouch & Mark H. Wright & Chih-Wei Tung & Lyza G. Maron & Kenneth L. McNally & Melissa Fitzgerald & Namrata Singh & Genevieve DeClerck & Francisco Agosto Perez & Pavel Korniliev & Anthony J., 2016. "Correction: Corrigendum: Open access resources for genome-wide association mapping in rice," Nature Communications, Nature, vol. 7(1), pages 1-1, September.
    5. Rico Gamuyao & Joong Hyoun Chin & Juan Pariasca-Tanaka & Paolo Pesaresi & Sheryl Catausan & Cheryl Dalid & Inez Slamet-Loedin & Evelyn Mae Tecson-Mendoza & Matthias Wissuwa & Sigrid Heuer, 2012. "The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency," Nature, Nature, vol. 488(7412), pages 535-539, August.
    6. Xuehui Huang & Nori Kurata & Xinghua Wei & Zi-Xuan Wang & Ahong Wang & Qiang Zhao & Yan Zhao & Kunyan Liu & Hengyun Lu & Wenjun Li & Yunli Guo & Yiqi Lu & Congcong Zhou & Danlin Fan & Qijun Weng & Chu, 2012. "A map of rice genome variation reveals the origin of cultivated rice," Nature, Nature, vol. 490(7421), pages 497-501, October.
    7. Agnieszka A. Golicz & Philipp E. Bayer & Guy C. Barker & Patrick P. Edger & HyeRan Kim & Paula A. Martinez & Chon Kit Kenneth Chan & Anita Severn-Ellis & W. Richard McCombie & Isobel A. P. Parkin & An, 2016. "The pangenome of an agronomically important crop plant Brassica oleracea," Nature Communications, Nature, vol. 7(1), pages 1-8, December.
    8. Kenong Xu & Xia Xu & Takeshi Fukao & Patrick Canlas & Reycel Maghirang-Rodriguez & Sigrid Heuer & Abdelbagi M. Ismail & Julia Bailey-Serres & Pamela C. Ronald & David J. Mackill, 2006. "Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice," Nature, Nature, vol. 442(7103), pages 705-708, August.
    9. 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.
    10. Susan R. McCouch & Mark H. Wright & Chih-Wei Tung & Lyza G. Maron & Kenneth L. McNally & Melissa Fitzgerald & Namrata Singh & Genevieve DeClerck & Francisco Agosto-Perez & Pavel Korniliev & Anthony J., 2016. "Open access resources for genome-wide association mapping in rice," Nature Communications, Nature, vol. 7(1), pages 1-14, April.
    11. 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.
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