IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43531-5.html
   My bibliography  Save this article

Building a eukaryotic chromosome arm by de novo design and synthesis

Author

Listed:
  • Shuangying Jiang

    (Chinese Academy of Sciences)

  • Zhouqing Luo

    (Chinese Academy of Sciences
    Xiamen University)

  • Jie Wu

    (Chinese Academy of Sciences)

  • Kang Yu

    (Chinese Academy of Sciences)

  • Shijun Zhao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Zelin Cai

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wenfei Yu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Hui Wang

    (Xiamen University)

  • Li Cheng

    (Chinese Academy of Sciences)

  • Zhenzhen Liang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Hui Gao

    (Chinese Academy of Sciences
    Shenzhen Bay Laboratory)

  • Marco Monti

    (University of Manchester)

  • Daniel Schindler

    (University of Manchester)

  • Linsen Huang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Cheng Zeng

    (Chinese Academy of Sciences)

  • Weimin Zhang

    (NYU Langone Health)

  • Chun Zhou

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yuanwei Tang

    (Chinese Academy of Sciences)

  • Tianyi Li

    (Chinese Academy of Sciences)

  • Yingxin Ma

    (Chinese Academy of Sciences)

  • Yizhi Cai

    (Chinese Academy of Sciences
    University of Manchester)

  • Jef D. Boeke

    (NYU Langone Health
    NYU Tandon School of Engineering)

  • Qiao Zhao

    (Chinese Academy of Sciences)

  • Junbiao Dai

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

Abstract

The genome of an organism is inherited from its ancestor and continues to evolve over time, however, the extent to which the current version could be altered remains unknown. To probe the genome plasticity of Saccharomyces cerevisiae, here we replace the native left arm of chromosome XII (chrXIIL) with a linear artificial chromosome harboring small sets of reconstructed genes. We find that as few as 12 genes are sufficient for cell viability, whereas 25 genes are required to recover the partial fitness defects observed in the 12-gene strain. Next, we demonstrate that these genes can be reconstructed individually using synthetic regulatory sequences and recoded open-reading frames with a “one-amino-acid-one-codon” strategy to remain functional. Finally, a synthetic neochromsome with the reconstructed genes is assembled which could substitute chrXIIL for viability. Together, our work not only highlights the high plasticity of yeast genome, but also illustrates the possibility of making functional eukaryotic chromosomes from entirely artificial sequences.

Suggested Citation

  • Shuangying Jiang & Zhouqing Luo & Jie Wu & Kang Yu & Shijun Zhao & Zelin Cai & Wenfei Yu & Hui Wang & Li Cheng & Zhenzhen Liang & Hui Gao & Marco Monti & Daniel Schindler & Linsen Huang & Cheng Zeng &, 2023. "Building a eukaryotic chromosome arm by de novo design and synthesis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43531-5
    DOI: 10.1038/s41467-023-43531-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43531-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43531-5?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. Jingchuan Luo & Xiaoji Sun & Brendan P. Cormack & Jef D. Boeke, 2018. "Karyotype engineering by chromosome fusion leads to reproductive isolation in yeast," Nature, Nature, vol. 560(7718), pages 392-396, August.
    2. Heidi Redden & Hal S. Alper, 2015. "The development and characterization of synthetic minimal yeast promoters," Nature Communications, Nature, vol. 6(1), pages 1-9, November.
    3. Julius Fredens & Kaihang Wang & Daniel Torre & Louise F. H. Funke & Wesley E. Robertson & Yonka Christova & Tiongsun Chia & Wolfgang H. Schmied & Daniel L. Dunkelmann & Václav Beránek & Chayasith Utta, 2019. "Total synthesis of Escherichia coli with a recoded genome," Nature, Nature, vol. 569(7757), pages 514-518, May.
    4. Jessica S. Dymond & Sarah M. Richardson & Candice E. Coombes & Timothy Babatz & Héloïse Muller & Narayana Annaluru & William J. Blake & Joy W. Schwerzmann & Junbiao Dai & Derek L. Lindstrom & Annabel , 2011. "Synthetic chromosome arms function in yeast and generate phenotypic diversity by design," Nature, Nature, vol. 477(7365), pages 471-476, September.
    5. Parithi Balachandran & Isha A. Walawalkar & Jacob I. Flores & Jacob N. Dayton & Peter A. Audano & Christine R. Beck, 2022. "Transposable element-mediated rearrangements are prevalent in human genomes," Nature Communications, Nature, vol. 13(1), pages 1-14, 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. Alessandro L. V. Coradini & Christopher Ne Ville & Zachary A. Krieger & Joshua Roemer & Cara Hull & Shawn Yang & Daniel T. Lusk & Ian M. Ehrenreich, 2023. "Building synthetic chromosomes from natural DNA," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Yuting Chen & Eriona Hysolli & Anlu Chen & Stephen Casper & Songlei Liu & Kevin Yang & Chenli Liu & George Church, 2022. "Multiplex base editing to convert TAG into TAA codons in the human genome," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Huiming Zhang & Xian Fu & Xuemei Gong & Yun Wang & Haolin Zhang & Yu Zhao & Yue Shen, 2022. "Systematic dissection of key factors governing recombination outcomes by GCE-SCRaMbLE," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Inbal Vaknin & Or Willinger & Jonathan Mandl & Hadar Heuberger & Dan Ben-Ami & Yi Zeng & Sarah Goldberg & Yaron Orenstein & Roee Amit, 2024. "A universal system for boosting gene expression in eukaryotic cell-lines," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Marine Duhamel & Michael E. Hood & Ricardo C. Rodríguez de la Vega & Tatiana Giraud, 2023. "Dynamics of transposable element accumulation in the non-recombining regions of mating-type chromosomes in anther-smut fungi," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Hideto Mori & Nozomu Yachie, 2022. "A framework to efficiently describe and share reproducible DNA materials and construction protocols," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    7. Charlotte Cautereels & Jolien Smets & Peter Bircham & Dries De Ruysscher & Anna Zimmermann & Peter De Rijk & Jan Steensels & Anton Gorkovskiy & Joleen Masschelein & Kevin J. Verstrepen, 2024. "Combinatorial optimization of gene expression through recombinase-mediated promoter and terminator shuffling in yeast," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Kang Hu & Peng Ni & Minghua Xu & You Zou & Jianye Chang & Xin Gao & Yaohang Li & Jue Ruan & Bin Hu & Jianxin Wang, 2024. "HiTE: a fast and accurate dynamic boundary adjustment approach for full-length transposable element detection and annotation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Tiantian Chang & Weichao Ding & Shirui Yan & Yun Wang & Haoling Zhang & Yu Zhang & Zhi Ping & Huiming Zhang & Yijian Huang & Jiahui Zhang & Dan Wang & Wenwei Zhang & Xun Xu & Yue Shen & Xian Fu, 2023. "A robust yeast biocontainment system with two-layered regulation switch dependent on unnatural amino acid," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Alessia Russo & Mattia Alessandrini & Moaine El Baidouri & Daniel Frei & Teresa Rosa Galise & Lara Gaidusch & Hannah F. Oertel & Sara E. Garcia Morales & Giacomo Potente & Qin Tian & Dmitry Smetanin &, 2024. "Genome of the early spider-orchid Ophrys sphegodes provides insights into sexual deception and pollinator adaptation," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    11. Donghui Choe & Connor A. Olson & Richard Szubin & Hannah Yang & Jaemin Sung & Adam M. Feist & Bernhard O. Palsson, 2024. "Advancing the scale of synthetic biology via cross-species transfer of cellular functions enabled by iModulon engraftment," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    12. Wolfram Höps & Tobias Rausch & Michael Jendrusch & Jan O. Korbel & Fritz J. Sedlazeck, 2024. "Impact and characterization of serial structural variations across humans and great apes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    13. Li Cheng & Shijun Zhao & Tianyi Li & Sha Hou & Zhouqing Luo & Jinsheng Xu & Wenfei Yu & Shuangying Jiang & Marco Monti & Daniel Schindler & Weimin Zhang & Chunhui Hou & Yingxin Ma & Yizhi Cai & Jef D., 2024. "Large-scale genomic rearrangements boost SCRaMbLE in Saccharomyces cerevisiae," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    14. Zhichao Zhang & Xiaoyi Zhang & Yuan Tian & Liyuan Wang & Jingting Cao & Hui Feng & Kainan Li & Yan Wang & Suomeng Dong & Wenwu Ye & Yuanchao Wang, 2024. "Complete telomere-to-telomere genomes uncover virulence evolution conferred by chromosome fusion in oomycete plant pathogens," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    15. Jan Zrimec & Xiaozhi Fu & Azam Sheikh Muhammad & Christos Skrekas & Vykintas Jauniskis & Nora K. Speicher & Christoph S. Börlin & Vilhelm Verendel & Morteza Haghir Chehreghani & Devdatt Dubhashi & Ver, 2022. "Controlling gene expression with deep generative design of regulatory DNA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    16. Dariusz R. Kutyna & Cristobal A. Onetto & Thomas C. Williams & Hugh D. Goold & Ian T. Paulsen & Isak S. Pretorius & Daniel L. Johnson & Anthony R. Borneman, 2022. "Construction of a synthetic Saccharomyces cerevisiae pan-genome neo-chromosome," Nature Communications, Nature, vol. 13(1), pages 1-9, 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:14:y:2023:i:1:d:10.1038_s41467-023-43531-5. 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.