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Comprehensive mapping and modelling of the rice regulome landscape unveils the regulatory architecture underlying complex traits

Author

Listed:
  • Tao Zhu

    (Nanjing University
    Nanjing University)

  • Chunjiao Xia

    (Huazhong Agricultural University)

  • Ranran Yu

    (Nanjing University)

  • Xinkai Zhou

    (Nanjing University)

  • Xingbing Xu

    (Huazhong Agricultural University)

  • Lin Wang

    (Nanjing University)

  • Zhanxiang Zong

    (Huazhong Agricultural University)

  • Junjiao Yang

    (Huazhong Agricultural University)

  • Yinmeng Liu

    (Huazhong Agricultural University)

  • Luchang Ming

    (Huazhong Agricultural University)

  • Yuxin You

    (Nanjing University)

  • Dijun Chen

    (Nanjing University
    Nanjing University)

  • Weibo Xie

    (Huazhong Agricultural University
    Huazhong Agricultural University
    Chinese Academy of Agricultural Sciences)

Abstract

Unraveling the regulatory mechanisms that govern complex traits is pivotal for advancing crop improvement. Here we present a comprehensive regulome atlas for rice (Oryza sativa), charting the chromatin accessibility across 23 distinct tissues from three representative varieties. Our study uncovers 117,176 unique open chromatin regions (OCRs), accounting for ~15% of the rice genome, a notably higher proportion compared to previous reports in plants. Integrating RNA-seq data from matched tissues, we confidently predict 59,075 OCR-to-gene links, with enhancers constituting 69.54% of these associations, including many known enhancer-to-gene links. Leveraging this resource, we re-evaluate genome-wide association study results and discover a previously unknown function of OsbZIP06 in seed germination, which we subsequently confirm through experimental validation. We optimize deep learning models to decode regulatory grammar, achieving robust modeling of tissue-specific chromatin accessibility. This approach allows to predict cross-variety regulatory dynamics from genomic sequences, shedding light on the genetic underpinnings of cis-regulatory divergence and morphological disparities between varieties. Overall, our study establishes a foundational resource for rice functional genomics and precision molecular breeding, providing valuable insights into regulatory mechanisms governing complex traits.

Suggested Citation

  • Tao Zhu & Chunjiao Xia & Ranran Yu & Xinkai Zhou & Xingbing Xu & Lin Wang & Zhanxiang Zong & Junjiao Yang & Yinmeng Liu & Luchang Ming & Yuxin You & Dijun Chen & Weibo Xie, 2024. "Comprehensive mapping and modelling of the rice regulome landscape unveils the regulatory architecture underlying complex traits," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50787-y
    DOI: 10.1038/s41467-024-50787-y
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    References listed on IDEAS

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    1. Liang-Yu Fu & Tao Zhu & Xinkai Zhou & Ranran Yu & Zhaohui He & Peijing Zhang & Zhigui Wu & Ming Chen & Kerstin Kaufmann & Dijun Chen, 2022. "ChIP-Hub provides an integrative platform for exploring plant regulome," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Lin Zhang & Hong Yu & Bin Ma & Guifu Liu & Jianjun Wang & Junmin Wang & Rongcun Gao & Jinjun Li & Jiyun Liu & Jing Xu & Yingying Zhang & Qun Li & Xuehui Huang & Jianlong Xu & Jianming Li & Qian Qian &, 2017. "A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice," Nature Communications, Nature, vol. 8(1), pages 1-10, April.
    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. Mette Bentsen & Philipp Goymann & Hendrik Schultheis & Kathrin Klee & Anastasiia Petrova & René Wiegandt & Annika Fust & Jens Preussner & Carsten Kuenne & Thomas Braun & Johnny Kim & Mario Looso, 2020. "ATAC-seq footprinting unravels kinetics of transcription factor binding during zygotic genome activation," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    5. Xingming Sun & Haiyan Xiong & Conghui Jiang & Dongmei Zhang & Zengling Yang & Yuanping Huang & Wanbin Zhu & Shuaishuai Ma & Junzhi Duan & Xin Wang & Wei Liu & Haifeng Guo & Gangling Li & Jiawei Qi & C, 2022. "Natural variation of DROT1 confers drought adaptation in upland rice," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. Rujia Chen & Ning Xiao & Yue Lu & Tianyun Tao & Qianfeng Huang & Shuting Wang & Zhichao Wang & Mingli Chuan & Qing Bu & Zhou Lu & Hanyao Wang & Yanze Su & Yi Ji & Jianheng Ding & Ahmed Gharib & Huixin, 2023. "A de novo evolved gene contributes to rice grain shape difference between indica and japonica," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Luchang Ming & Debao Fu & Zhaona Wu & Hu Zhao & Xingbing Xu & Tingting Xu & Xiaohu Xiong & Mu Li & Yi Zheng & Ge Li & Ling Yang & Chunjiao Xia & Rongfang Zhou & Keyan Liao & Qian Yu & Wenqi Chai & Sij, 2023. "Transcriptome-wide association analyses reveal the impact of regulatory variants on rice panicle architecture and causal gene regulatory networks," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
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