IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50787-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50787-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-50787-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    4. 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.
    5. 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.
    6. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Huiying He & Yue Leng & Xinglan Cao & Yiwang Zhu & Xiaoxia Li & Qiaoling Yuan & Bin Zhang & Wenchuang He & Hua Wei & Xiangpei Liu & Qiang Xu & Mingliang Guo & Hong Zhang & Longbo Yang & Yang Lv & Xian, 2024. "The pan-tandem repeat map highlights multiallelic variants underlying gene expression and agronomic traits in rice," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Qianjin Liang & Liyu Chen & Xia Yang & Hui Yang & Shulin Liu & Kun Kou & Lei Fan & Zhifang Zhang & Zongbiao Duan & Yaqin Yuan & Shan Liang & Yucheng Liu & Xingtong Lu & Guoan Zhou & Min Zhang & Fanjia, 2022. "Natural variation of Dt2 determines branching in soybean," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    3. Hideki Yoshida & Ko Hirano & Kenji Yano & Fanmiao Wang & Masaki Mori & Mayuko Kawamura & Eriko Koketsu & Masako Hattori & Reynante Lacsamana Ordonio & Peng Huang & Eiji Yamamoto & Makoto Matsuoka, 2022. "Genome-wide association study identifies a gene responsible for temperature-dependent rice germination," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Yu Chen & Amy Y. Wang & Courtney A. Barkley & Yixin Zhang & Xinyang Zhao & Min Gao & Mick D. Edmonds & Zechen Chong, 2023. "Deciphering the exact breakpoints of structural variations using long sequencing reads with DeBreak," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. 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.
    6. Felicia Lazure & Rick Farouni & Korin Sahinyan & Darren M. Blackburn & Aldo Hernández-Corchado & Gabrielle Perron & Tianyuan Lu & Adrien Osakwe & Jiannis Ragoussis & Colin Crist & Theodore J. Perkins , 2023. "Transcriptional reprogramming of skeletal muscle stem cells by the niche environment," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Yingyan Yu & Zhen Zhang & Xiaorui Dong & Ruixin Yang & Zhongqu Duan & Zhen Xiang & Jun Li & Guichao Li & Fazhe Yan & Hongzhang Xue & Du Jiao & Jinyuan Lu & Huimin Lu & Wenmin Zhang & Yangzhen Wei & Sh, 2022. "Pangenomic analysis of Chinese gastric cancer," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. Fuxi Rong & Yusong Lv & Pingchuan Deng & Xia Wu & Yaqi Zhang & Erkui Yue & Yuxin Shen & Sajid Muhammad & Fangrui Ni & Hongwu Bian & Xiangjin Wei & Weijun Zhou & Peisong Hu & Liang Wu, 2024. "Switching action modes of miR408-5p mediates auxin signaling in rice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    9. 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.
    10. Kathleen Shah & Muralidhara Rao Maradana & M. Joaquina Delàs & Amina Metidji & Frederike Graelmann & Miriam Llorian & Probir Chakravarty & Ying Li & Mauro Tolaini & Michael Shapiro & Gavin Kelly & Chr, 2022. "Cell-intrinsic Aryl Hydrocarbon Receptor signalling is required for the resolution of injury-induced colonic stem cells," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    11. Ashton S. Holub & Sarah G. Choudury & Ekaterina P. Andrianova & Courtney E. Dresden & Ricardo Urquidi Camacho & Igor B. Zhulin & Aman Y. Husbands, 2024. "START domains generate paralog-specific regulons from a single network architecture," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    12. Xiaojuan Fan & Yongtao Cui & Jian Song & Honghuan Fan & Liqun Tang & Jianjun Wang, 2024. "Preliminary Exploration of Physiology and Genetic Basis Underlying High Yield in Indica–Japonica Hybrid Rice," Agriculture, MDPI, vol. 14(4), pages 1-12, April.
    13. Zhenhui Zhong & Yafei Wang & Ming Wang & Fan Yang & Quentin Angelo Thomas & Yan Xue & Yaxin Zhang & Wanlu Liu & Yasaman Jami-Alahmadi & Linhao Xu & Suhua Feng & Sebastian Marquardt & James A. Wohlschl, 2022. "Histone chaperone ASF1 mediates H3.3-H4 deposition in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Dhurjhoti Saha & Solomon Hailu & Arjan Hada & Junwoo Lee & Jie Luo & Jeff A. Ranish & Yuan-chi Lin & Kyle Feola & Jim Persinger & Abhinav Jain & Bin Liu & Yue Lu & Payel Sen & Blaine Bartholomew, 2023. "The AT-hook is an evolutionarily conserved auto-regulatory domain of SWI/SNF required for cell lineage priming," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Joyce J. Thompson & Daniel J. Lee & Apratim Mitra & Sarah Frail & Ryan K. Dale & Pedro P. Rocha, 2022. "Extensive co-binding and rapid redistribution of NANOG and GATA6 during emergence of divergent lineages," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    16. Ting Wang & Shiyao Duan & Chen Xu & Yi Wang & Xinzhong Zhang & Xuefeng Xu & Liyang Chen & Zhenhai Han & Ting Wu, 2023. "Pan-genome analysis of 13 Malus accessions reveals structural and sequence variations associated with fruit traits," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Yakun Wang & Shengjia Tang & Naihui Guo & Ruihu An & Zongliang Ren & Shikai Hu & Xiangjin Wei & Guiai Jiao & Lihong Xie & Ling Wang & Ying Chen & Fengli Zhao & Peisong Hu & Zhonghua Sheng & Shaoqing T, 2023. "Base Editing of EUI1 Improves the Elongation of the Uppermost Internode in Two-Line Male Sterile Rice Lines," Agriculture, MDPI, vol. 13(3), pages 1-13, March.
    18. Moritz Binder & Raphael E. Szalat & Srikanth Talluri & Mariateresa Fulciniti & Hervé Avet-Loiseau & Giovanni Parmigiani & Mehmet K. Samur & Nikhil C. Munshi, 2024. "Bone marrow stromal cells induce chromatin remodeling in multiple myeloma cells leading to transcriptional changes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    19. Hui Shi & Junjie Yin & Zhangjie Zhao & Hong Yu & Hong Yi & Li Xu & Huimin Tong & Min He & Xiaobo Zhu & Xiang Lu & Qing Xiong & Weitao Li & Yongyan Tang & Qingqing Hou & Li Song & Long Wang & Xiaoqiong, 2024. "Fine-tuning of IPA1 transactivation activity by E3 ligase IPI7-mediated non-proteolytic K29-ubiquitination during Magnaporthe oryzae infection," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    20. Timothy D. Arthur & Jennifer P. Nguyen & Agnieszka D’Antonio-Chronowska & Hiroko Matsui & Nayara S. Silva & Isaac N. Joshua & André D. Luchessi & William W. Young Greenwald & Matteo D’Antonio & Martin, 2024. "Complex regulatory networks influence pluripotent cell state transitions in human iPSCs," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50787-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.