IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46780-0.html
   My bibliography  Save this article

Temporospatial hierarchy and allele-specific expression of zygotic genome activation revealed by distant interspecific urochordate hybrids

Author

Listed:
  • Jiankai Wei

    (Ocean University of China
    Qingdao Marine Science and Technology Center
    Ocean University of China)

  • Wei Zhang

    (Ocean University of China)

  • An Jiang

    (Ocean University of China)

  • Hongzhe Peng

    (Ocean University of China)

  • Quanyong Zhang

    (Kunming University of Science and Technology)

  • Yuting Li

    (Ocean University of China)

  • Jianqing Bi

    (Ocean University of China)

  • Linting Wang

    (Chinese Academy of Sciences)

  • Penghui Liu

    (Ocean University of China)

  • Jing Wang

    (Ocean University of China)

  • Yonghang Ge

    (Ocean University of China)

  • Liya Zhang

    (Kunming University of Science and Technology)

  • Haiyan Yu

    (Ocean University of China)

  • Lei Li

    (Chinese Academy of Sciences)

  • Shi Wang

    (Ocean University of China
    Qingdao Marine Science and Technology Center)

  • Liang Leng

    (Chengdu University of Traditional Chinese Medicine)

  • Kai Chen

    (Kunming University of Science and Technology
    Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou))

  • Bo Dong

    (Ocean University of China
    Qingdao Marine Science and Technology Center
    Ocean University of China)

Abstract

Zygotic genome activation (ZGA) is a universal process in early embryogenesis of metazoan, when the quiescent zygotic nucleus initiates global transcription. However, the mechanisms related to massive genome activation and allele-specific expression (ASE) remain not well understood. Here, we develop hybrids from two deeply diverged (120 Mya) ascidian species to symmetrically document the dynamics of ZGA. We identify two coordinated ZGA waves represent early developmental and housekeeping gene reactivation, respectively. Single-cell RNA sequencing reveals that the major expression wave exhibits spatial heterogeneity and significantly correlates with cell fate. Moreover, allele-specific expression occurs in a species- rather than parent-related manner, demonstrating the divergence of cis-regulatory elements between the two species. These findings provide insights into ZGA in chordates.

Suggested Citation

  • Jiankai Wei & Wei Zhang & An Jiang & Hongzhe Peng & Quanyong Zhang & Yuting Li & Jianqing Bi & Linting Wang & Penghui Liu & Jing Wang & Yonghang Ge & Liya Zhang & Haiyan Yu & Lei Li & Shi Wang & Liang, 2024. "Temporospatial hierarchy and allele-specific expression of zygotic genome activation revealed by distant interspecific urochordate hybrids," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46780-0
    DOI: 10.1038/s41467-024-46780-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46780-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-46780-0?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. Chen Cao & Laurence A. Lemaire & Wei Wang & Peter H. Yoon & Yoolim A. Choi & Lance R. Parsons & John C. Matese & Wei Wang & Michael Levine & Kai Chen, 2019. "Comprehensive single-cell transcriptome lineages of a proto-vertebrate," Nature, Nature, vol. 571(7765), pages 349-354, July.
    2. Michael D. Nodine & David P. Bartel, 2012. "Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos," Nature, Nature, vol. 482(7383), pages 94-97, February.
    3. Saartje Hontelez & Ila van Kruijsbergen & Georgios Georgiou & Simon J. van Heeringen & Ozren Bogdanovic & Ryan Lister & Gert Jan C. Veenstra, 2015. "Embryonic transcription is controlled by maternally defined chromatin state," Nature Communications, Nature, vol. 6(1), pages 1-13, December.
    4. Carsten Grashoff & Brenton D. Hoffman & Michael D. Brenner & Ruobo Zhou & Maddy Parsons & Michael T. Yang & Mark A. McLean & Stephen G. Sligar & Christopher S. Chen & Taekjip Ha & Martin A. Schwartz, 2010. "Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics," Nature, Nature, vol. 466(7303), pages 263-266, July.
    5. Gerardo Del Toro-De León & Marcelina García-Aguilar & C. Stewart Gillmor, 2014. "Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis," Nature, Nature, vol. 514(7524), pages 624-627, October.
    6. Nadine L. Vastenhouw & Yong Zhang & Ian G. Woods & Farhad Imam & Aviv Regev & X. Shirley Liu & John Rinn & Alexander F. Schier, 2010. "Chromatin signature of embryonic pluripotency is established during genome activation," Nature, Nature, vol. 464(7290), pages 922-926, April.
    7. Emily S. Wong & Bianca M. Schmitt & Anastasiya Kazachenka & David Thybert & Aisling Redmond & Frances Connor & Tim F. Rayner & Christine Feig & Anne C. Ferguson-Smith & John C. Marioni & Duncan T. Odo, 2017. "Interplay of cis and trans mechanisms driving transcription factor binding and gene expression evolution," Nature Communications, Nature, vol. 8(1), pages 1-13, 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. Sarah E. Harris & Maria S. Alexis & Gilbert Giri & Francisco F. Cavazos & Yue Hu & Jernej Murn & Maria M. Aleman & Christopher B. Burge & Daniel Dominguez, 2024. "Understanding species-specific and conserved RNA-protein interactions in vivo and in vitro," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. B. Kempisty & D. Bukowska & H. Piotrowska & P. Zawierucha & P. Sniadek & R. Walczak & J. Dziuban & P. Antosik & J. Jaskowski & K.P. Brussow & M. Nowicki & M. Zabel, 2011. "Selected molecular and microfluidic aspects of mammalian oocyte maturation-perspectives: a review," Veterinární medicína, Czech Academy of Agricultural Sciences, vol. 56(8), pages 367-378.
    3. Zhijun Dong & Fanghan Wang & Yali Liu & Yongxue Li & Haiyan Yu & Saijun Peng & Tingting Sun & Meng Qu & Ke Sun & Lei Wang & Yuanqing Ma & Kai Chen & Jianmin Zhao & Qiang Lin, 2024. "Genomic and single-cell analyses reveal genetic signatures of swimming pattern and diapause strategy in jellyfish," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Hong Wang & Rayan Said & Clémence Nguyen-Vigouroux & Véronique Henriot & Peter Gebhardt & Julien Pernier & Robert Grosse & Christophe Le Clainche, 2024. "Talin and vinculin combine their activities to trigger actin assembly," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Toshio Sekiguchi & Hiroshi Akitaya & Satoshi Nakayama & Takashi Yazawa & Michio Ogasawara & Nobuo Suzuki & Kazuichi Hayakawa & Shuichi Wada, 2020. "Effect of Polycyclic Aromatic Hydrocarbons on Development of the Ascidian Ciona intestinalis Type A," IJERPH, MDPI, vol. 17(4), pages 1-11, February.
    6. Meijiang Gao & Marina Veil & Marcus Rosenblatt & Aileen Julia Riesle & Anna Gebhard & Helge Hass & Lenka Buryanova & Lev Y. Yampolsky & Björn Grüning & Sergey V. Ulianov & Jens Timmer & Daria Onichtch, 2022. "Pluripotency factors determine gene expression repertoire at zygotic genome activation," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    7. Shixuan Liu & Camille Ezran & Michael F. Z. Wang & Zhengda Li & Kyle Awayan & Jonathan Z. Long & Iwijn De Vlaminck & Sheng Wang & Jacques Epelbaum & Christin S. Kuo & Jérémy Terrien & Mark A. Krasnow , 2024. "An organism-wide atlas of hormonal signaling based on the mouse lemur single-cell transcriptome," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
    8. Serena Petracchini & Daniel Hamaoui & Anne Doye & Atef Asnacios & Florian Fage & Elisa Vitiello & Martial Balland & Sebastien Janel & Frank Lafont & Mukund Gupta & Benoit Ladoux & Jerôme Gilleron & Te, 2022. "Optineurin links Hace1-dependent Rac ubiquitylation to integrin-mediated mechanotransduction to control bacterial invasion and cell division," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    9. Yuhang Zhang & Jingyi Du & Xian Liu & Fei Shang & Yunxin Deng & Jiaqing Ye & Yukai Wang & Jie Yan & Hu Chen & Miao Yu & Shimin Le, 2024. "Multi-domain interaction mediated strength-building in human α-actinin dimers unveiled by direct single-molecule quantification," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. Venkat R. Chirasani & Mohammad Ashhar I. Khan & Juilee N. Malavade & Nikolay V. Dokholyan & Brenton D. Hoffman & Sharon L. Campbell, 2023. "Molecular basis and cellular functions of vinculin-actin directional catch bonding," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    11. Matthew R. Pawlak & Adam T. Smiley & Maria Paz Ramirez & Marcus D. Kelly & Ghaidan A. Shamsan & Sarah M. Anderson & Branden A. Smeester & David A. Largaespada & David J. Odde & Wendy R. Gordon, 2023. "RAD-TGTs: high-throughput measurement of cellular mechanotype via rupture and delivery of DNA tension probes," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    12. Martin Arostegui & R. Wilder Scott & Kerstin Böse & T. Michael Underhill, 2022. "Cellular taxonomy of Hic1+ mesenchymal progenitor derivatives in the limb: from embryo to adult," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    13. Md Tauhidul Islam & Lei Xing, 2023. "Cartography of Genomic Interactions Enables Deep Analysis of Single-Cell Expression Data," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Brooke E. Danielsson & Bobin George Abraham & Elina Mäntylä & Jolene I. Cabe & Carl R. Mayer & Anna Rekonen & Frans Ek & Daniel E. Conway & Teemu O. Ihalainen, 2023. "Nuclear lamina strain states revealed by intermolecular force biosensor," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    15. Shifeng Xue & Thanh Thao Nguyen Ly & Raunak S. Vijayakar & Jingyi Chen & Joel Ng & Ajay S. Mathuru & Frederique Magdinier & Bruno Reversade, 2022. "HOX epimutations driven by maternal SMCHD1/LRIF1 haploinsufficiency trigger homeotic transformations in genetically wildtype offspring," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    16. Kaitlyn A. Lagattuta & Hannah L. Park & Laurie Rumker & Kazuyoshi Ishigaki & Aparna Nathan & Soumya Raychaudhuri, 2024. "The genetic basis of autoimmunity seen through the lens of T cell functional traits," Nature Communications, Nature, vol. 15(1), pages 1-6, December.
    17. Chrystian Junqueira Alves & Rafael Dariolli & Jonathan Haydak & Sangjo Kang & Theodore Hannah & Robert J. Wiener & Stefanie DeFronzo & Rut Tejero & Gabriele L. Gusella & Aarthi Ramakrishnan & Rodrigo , 2021. "Plexin-B2 orchestrates collective stem cell dynamics via actomyosin contractility, cytoskeletal tension and adhesion," Nature Communications, Nature, vol. 12(1), pages 1-23, December.
    18. Yuan Liao & Lifeng Ma & Qile Guo & Weigao E & Xing Fang & Lei Yang & Fanwei Ruan & Jingjing Wang & Peijing Zhang & Zhongyi Sun & Haide Chen & Zhongliang Lin & Xueyi Wang & Xinru Wang & Huiyu Sun & Xiu, 2022. "Cell landscape of larval and adult Xenopus laevis at single-cell resolution," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    19. Xavier Grau-Bové & Lucie Subirana & Lydvina Meister & Anaël Soubigou & Ana Neto & Anamaria Elek & Silvia Naranjo & Oscar Fornas & Jose Luis Gomez-Skarmeta & Juan J. Tena & Manuel Irimia & Stéphanie Be, 2024. "An amphioxus neurula stage cell atlas supports a complex scenario for the emergence of vertebrate head mesoderm," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    20. Thao Nguyen & Eli J. Costa & Tim Deibert & Jose Reyes & Felix C. Keber & Miroslav Tomschik & Michael Stadlmeier & Meera Gupta & Chirag K. Kumar & Edward R. Cruz & Amanda Amodeo & Jesse C. Gatlin & Mar, 2022. "Differential nuclear import sets the timing of protein access to the embryonic genome," Nature Communications, Nature, vol. 13(1), pages 1-16, 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_s41467-024-46780-0. 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.