IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29561-5.html
   My bibliography  Save this article

Reshuffling of the ancestral core-eudicot genome shaped chromatin topology and epigenetic modification in Panax

Author

Listed:
  • Zhen-Hui Wang

    (Jilin Agricultural University
    Fudan University
    Northeast Normal University)

  • Xin-Feng Wang

    (Fudan University)

  • Tianyuan Lu

    (McGill University and Genome Quebec Innovation Center)

  • Ming-Rui Li

    (Fudan University)

  • Peng Jiang

    (Northeast Normal University)

  • Jing Zhao

    (Northeast Normal University)

  • Si-Tong Liu

    (Jilin University)

  • Xue-Qi Fu

    (Jilin University)

  • Jonathan F. Wendel

    (Iowa State University)

  • Yves Peer

    (Ghent University and VIB Center for Plant Systems Biology
    University of Pretoria
    Nanjing Agricultural University)

  • Bao Liu

    (Northeast Normal University)

  • Lin-Feng Li

    (Fudan University)

Abstract

All extant core-eudicot plants share a common ancestral genome that has experienced cyclic polyploidizations and (re)diploidizations. Reshuffling of the ancestral core-eudicot genome generates abundant genomic diversity, but the role of this diversity in shaping the hierarchical genome architecture, such as chromatin topology and gene expression, remains poorly understood. Here, we assemble chromosome-level genomes of one diploid and three tetraploid Panax species and conduct in-depth comparative genomic and epigenomic analyses. We show that chromosomal interactions within each duplicated ancestral chromosome largely maintain in extant Panax species, albeit experiencing ca. 100–150 million years of evolution from a shared ancestor. Biased genetic fractionation and epigenetic regulation divergence during polyploidization/(re)diploidization processes generate remarkable biochemical diversity of secondary metabolites in the Panax genus. Our study provides a paleo-polyploidization perspective of how reshuffling of the ancestral core-eudicot genome leads to a highly dynamic genome and to the metabolic diversification of extant eudicot plants.

Suggested Citation

  • Zhen-Hui Wang & Xin-Feng Wang & Tianyuan Lu & Ming-Rui Li & Peng Jiang & Jing Zhao & Si-Tong Liu & Xue-Qi Fu & Jonathan F. Wendel & Yves Peer & Bao Liu & Lin-Feng Li, 2022. "Reshuffling of the ancestral core-eudicot genome shaped chromatin topology and epigenetic modification in Panax," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29561-5
    DOI: 10.1038/s41467-022-29561-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29561-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-29561-5?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. Xinyue Zhao & Jingrui Li & Bi Lian & Hanqing Gu & Yan Li & Yijun Qi, 2018. "Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Jesse R. Dixon & Siddarth Selvaraj & Feng Yue & Audrey Kim & Yan Li & Yin Shen & Ming Hu & Jun S. Liu & Bing Ren, 2012. "Topological domains in mammalian genomes identified by analysis of chromatin interactions," Nature, Nature, vol. 485(7398), pages 376-380, May.
    3. Andrew H. Paterson & Jonathan F. Wendel & Heidrun Gundlach & Hui Guo & Jerry Jenkins & Dianchuan Jin & Danny Llewellyn & Kurtis C. Showmaker & Shengqiang Shu & Joshua Udall & Mi-jeong Yoo & Robert Bye, 2012. "Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres," Nature, Nature, vol. 492(7429), pages 423-427, December.
    4. Karel Miettinen & Jacob Pollier & Dieter Buyst & Philipp Arendt & René Csuk & Sven Sommerwerk & Tessa Moses & Jan Mertens & Prashant D Sonawane & Laurens Pauwels & Asaph Aharoni & José Martins & David, 2017. "The ancient CYP716 family is a major contributor to the diversification of eudicot triterpenoid biosynthesis," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    5. Sebastian Reyes-Chin-Wo & Zhiwen Wang & Xinhua Yang & Alexander Kozik & Siwaret Arikit & Chi Song & Liangfeng Xia & Lutz Froenicke & Dean O. Lavelle & María-José Truco & Rui Xia & Shilin Zhu & Chunyan, 2017. "Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce," Nature Communications, Nature, vol. 8(1), pages 1-11, April.
    6. Emily Crane & Qian Bian & Rachel Patton McCord & Bryan R. Lajoie & Bayly S. Wheeler & Edward J. Ralston & Satoru Uzawa & Job Dekker & Barbara J. Meyer, 2015. "Condensin-driven remodelling of X chromosome topology during dosage compensation," Nature, Nature, vol. 523(7559), pages 240-244, July.
    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. Chong Wang & Xiang Liu & Jun Liang & Yohei Narita & Weiyue Ding & Difei Li & Luyao Zhang & Hongbo Wang & Merrin Man Long Leong & Isabella Hou & Catherine Gerdt & Chang Jiang & Qian Zhong & Zhonghui Ta, 2023. "A DNA tumor virus globally reprograms host 3D genome architecture to achieve immortal growth," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Ryuichiro Nakato & Toyonori Sakata & Jiankang Wang & Luis Augusto Eijy Nagai & Yuya Nagaoka & Gina Miku Oba & Masashige Bando & Katsuhiko Shirahige, 2023. "Context-dependent perturbations in chromatin folding and the transcriptome by cohesin and related factors," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Koon-Kiu Yan & Shaoke Lou & Mark Gerstein, 2017. "MrTADFinder: A network modularity based approach to identify topologically associating domains in multiple resolutions," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-22, July.
    4. Wu Zuo & Guangming Chen & Zhimei Gao & Shuai Li & Yanyan Chen & Chenhui Huang & Juan Chen & Zhengjun Chen & Ming Lei & Qian Bian, 2021. "Stage-resolved Hi-C analyses reveal meiotic chromosome organizational features influencing homolog alignment," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    5. Li-Hsin Chang & Sourav Ghosh & Andrea Papale & Jennifer M. Luppino & Mélanie Miranda & Vincent Piras & Jéril Degrouard & Joanne Edouard & Mallory Poncelet & Nathan Lecouvreur & Sébastien Bloyer & Amél, 2023. "Multi-feature clustering of CTCF binding creates robustness for loop extrusion blocking and Topologically Associating Domain boundaries," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Mingsen Li & Huaxing Huang & Bofeng Wang & Shaoshuai Jiang & Huizhen Guo & Liqiong Zhu & Siqi Wu & Jiafeng Liu & Li Wang & Xihong Lan & Wang Zhang & Jin Zhu & Fuxi Li & Jieying Tan & Zhen Mao & Chunqi, 2022. "Comprehensive 3D epigenomic maps define limbal stem/progenitor cell function and identity," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Bob Zimmermann & Juan D. Montenegro & Sofia M. C. Robb & Whitney J. Fropf & Lukas Weilguny & Shuonan He & Shiyuan Chen & Jessica Lovegrove-Walsh & Eric M. Hill & Cheng-Yi Chen & Katerina Ragkousi & Da, 2023. "Topological structures and syntenic conservation in sea anemone genomes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Yuan Yin & Huizhong Fan & Botong Zhou & Yibo Hu & Guangyi Fan & Jinhuan Wang & Fan Zhou & Wenhui Nie & Chenzhou Zhang & Lin Liu & Zhenyu Zhong & Wenbo Zhu & Guichun Liu & Zeshan Lin & Chang Liu & Jion, 2021. "Molecular mechanisms and topological consequences of drastic chromosomal rearrangements of muntjac deer," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    9. Zhen Wah Tan & Enrico Guarnera & Igor N Berezovsky, 2018. "Exploring chromatin hierarchical organization via Markov State Modelling," PLOS Computational Biology, Public Library of Science, vol. 14(12), pages 1-35, December.
    10. Lina Zheng & Wei Wang, 2022. "Regulation associated modules reflect 3D genome modularity associated with chromatin activity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    11. Jacques Serizay & Cyril Matthey-Doret & Amaury Bignaud & Lyam Baudry & Romain Koszul, 2024. "Orchestrating chromosome conformation capture analysis with Bioconductor," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    12. Yanlin Zhang & Mathieu Blanchette, 2022. "Reference panel guided topological structure annotation of Hi-C data," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. Olivier Messina & Flavien Raynal & Julian Gurgo & Jean-Bernard Fiche & Vera Pancaldi & Marcelo Nollmann, 2023. "3D chromatin interactions involving Drosophila insulators are infrequent but preferential and arise before TADs and transcription," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    14. Riccardo Calandrelli & Xingzhao Wen & John Lalith Charles Richard & Zhifei Luo & Tri C. Nguyen & Chien-Ju Chen & Zhijie Qi & Shuanghong Xue & Weizhong Chen & Zhangming Yan & Weixin Wu & Kathia Zaleta-, 2023. "Genome-wide analysis of the interplay between chromatin-associated RNA and 3D genome organization in human cells," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Long Jin & Danyang Wang & Jiaman Zhang & Pengliang Liu & Yujie Wang & Yu Lin & Can Liu & Ziyin Han & Keren Long & Diyan Li & Yu Jiang & Guisen Li & Yu Zhang & Jingyi Bai & Xiaokai Li & Jing Li & Lu Lu, 2023. "Dynamic chromatin architecture of the porcine adipose tissues with weight gain and loss," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    16. Bobae Yang & Sueun Kim & Woong-Jae Jung & Kyungwoo Kim & Sugyung Kim & Yong-Jin Kim & Tae-Gyun Kim & Eun-Chong Lee & Jung-Sik Joo & Chae Gyu Park & Sumin Oh & Kyung Hyun Yoo & Hyoung-Pyo Kim, 2023. "CTCF controls three-dimensional enhancer network underlying the inflammatory response of bone marrow-derived dendritic cells," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    17. Markus Götz & Olivier Messina & Sergio Espinola & Jean-Bernard Fiche & Marcelo Nollmann, 2022. "Multiple parameters shape the 3D chromatin structure of single nuclei at the doc locus in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    18. Mariam Okhovat & Jake VanCampen & Kimberly A. Nevonen & Lana Harshman & Weiyu Li & Cora E. Layman & Samantha Ward & Jarod Herrera & Jackson Wells & Rory R. Sheng & Yafei Mao & Blaise Ndjamen & Ana C. , 2023. "TAD evolutionary and functional characterization reveals diversity in mammalian TAD boundary properties and function," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    19. Xiao Ge & Haiyan Huang & Keqi Han & Wangjie Xu & Zhaoxia Wang & Qiang Wu, 2023. "Outward-oriented sites within clustered CTCF boundaries are key for intra-TAD chromatin interactions and gene regulation," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    20. Sarah B. Reiff & Andrew J. Schroeder & Koray Kırlı & Andrea Cosolo & Clara Bakker & Luisa Mercado & Soohyun Lee & Alexander D. Veit & Alexander K. Balashov & Carl Vitzthum & William Ronchetti & Kent M, 2022. "The 4D Nucleome Data Portal as a resource for searching and visualizing curated nucleomics data," Nature Communications, Nature, vol. 13(1), pages 1-11, 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:13:y:2022:i:1:d:10.1038_s41467-022-29561-5. 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.