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Pan-genome inversion index reveals evolutionary insights into the subpopulation structure of Asian rice

Author

Listed:
  • Yong Zhou

    (King Abdullah University of Science and Technology (KAUST)
    University of Arizona)

  • Zhichao Yu

    (Huazhong Agricultural University)

  • Dmytro Chebotarov

    (International Rice Research Institute (IRRI), Los Baños)

  • Kapeel Chougule

    (Cold Spring Harbor Laboratory)

  • Zhenyuan Lu

    (Cold Spring Harbor Laboratory)

  • Luis F. Rivera

    (King Abdullah University of Science and Technology (KAUST))

  • Nagarajan Kathiresan

    (King Abdullah University of Science and Technology (KAUST))

  • Noor Al-Bader

    (King Abdullah University of Science and Technology (KAUST))

  • Nahed Mohammed

    (King Abdullah University of Science and Technology (KAUST))

  • Aseel Alsantely

    (King Abdullah University of Science and Technology (KAUST))

  • Saule Mussurova

    (King Abdullah University of Science and Technology (KAUST))

  • João Santos

    (King Abdullah University of Science and Technology (KAUST))

  • Manjula Thimma

    (King Abdullah University of Science and Technology (KAUST))

  • Maxim Troukhan

    (Persephone Software, LLC)

  • Alice Fornasiero

    (King Abdullah University of Science and Technology (KAUST))

  • Carl D. Green

    (King Abdullah University of Science and Technology (KAUST))

  • Dario Copetti

    (University of Arizona)

  • David Kudrna

    (University of Arizona)

  • Victor Llaca

    (Research and Development, Corteva Agriscience)

  • Mathias Lorieux

    (DIADE, University of Montpellier, CIRAD, IRD)

  • Andrea Zuccolo

    (King Abdullah University of Science and Technology (KAUST)
    Crop Science Research Center (CSRC), Scuola Superiore Sant’Anna)

  • Doreen Ware

    (Cold Spring Harbor Laboratory
    USDA ARS NEA Plant, Soil & Nutrition Laboratory Research Unit)

  • Kenneth McNally

    (International Rice Research Institute (IRRI), Los Baños)

  • Jianwei Zhang

    (University of Arizona
    Huazhong Agricultural University)

  • Rod A. Wing

    (King Abdullah University of Science and Technology (KAUST)
    University of Arizona
    International Rice Research Institute (IRRI), Los Baños)

Abstract

Understanding and exploiting genetic diversity is a key factor for the productive and stable production of rice. Here, we utilize 73 high-quality genomes that encompass the subpopulation structure of Asian rice (Oryza sativa), plus the genomes of two wild relatives (O. rufipogon and O. punctata), to build a pan-genome inversion index of 1769 non-redundant inversions that span an average of ~29% of the O. sativa cv. Nipponbare reference genome sequence. Using this index, we estimate an inversion rate of ~700 inversions per million years in Asian rice, which is 16 to 50 times higher than previously estimated for plants. Detailed analyses of these inversions show evidence of their effects on gene expression, recombination rate, and linkage disequilibrium. Our study uncovers the prevalence and scale of large inversions (≥100 bp) across the pan-genome of Asian rice and hints at their largely unexplored role in functional biology and crop performance.

Suggested Citation

  • Yong Zhou & Zhichao Yu & Dmytro Chebotarov & Kapeel Chougule & Zhenyuan Lu & Luis F. Rivera & Nagarajan Kathiresan & Noor Al-Bader & Nahed Mohammed & Aseel Alsantely & Saule Mussurova & João Santos & , 2023. "Pan-genome inversion index reveals evolutionary insights into the subpopulation structure of Asian rice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37004-y
    DOI: 10.1038/s41467-023-37004-y
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    References listed on IDEAS

    as
    1. Yonghui Wu & Prasanna R Bhat & Timothy J Close & Stefano Lonardi, 2008. "Efficient and Accurate Construction of Genetic Linkage Maps from the Minimum Spanning Tree of a Graph," PLOS Genetics, Public Library of Science, vol. 4(10), pages 1-11, October.
    2. 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.
    3. Michal Levy-Sakin & Steven Pastor & Yulia Mostovoy & Le Li & Alden K. Y. Leung & Jennifer McCaffrey & Eleanor Young & Ernest T. Lam & Alex R. Hastie & Karen H. Y. Wong & Claire Y. L. Chung & Walfred M, 2019. "Genome maps across 26 human populations reveal population-specific patterns of structural variation," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    4. Daniel C. Jeffares & Clemency Jolly & Mimoza Hoti & Doug Speed & Liam Shaw & Charalampos Rallis & Francois Balloux & Christophe Dessimoz & Jürg Bähler & Fritz J. Sedlazeck, 2017. "Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast," Nature Communications, Nature, vol. 8(1), pages 1-11, April.
    5. Lun Zhao & Liang Xie & Qing Zhang & Weizhi Ouyang & Li Deng & Pengpeng Guan & Meng Ma & Yue Li & Ying Zhang & Qin Xiao & Jingwen Zhang & Hongmeijuan Li & Shunyao Wang & Jiangwei Man & Zhilin Cao & Qin, 2020. "Integrative analysis of reference epigenomes in 20 rice varieties," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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    1. Zeyu Zheng & Mingjia Zhu & Jin Zhang & Xinfeng Liu & Liqiang Hou & Wenyu Liu & Shuai Yuan & Changhong Luo & Xinhao Yao & Jianquan Liu & Yongzhi Yang, 2024. "A sequence-aware merger of genomic structural variations at population scale," Nature Communications, Nature, vol. 15(1), pages 1-9, December.

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