Zygotic gene activation in the chicken occurs in two waves, the first involving only maternally derived genes

  1. Young Sun Hwang
  2. Minseok Seo
  3. Sang Kyung Kim
  4. Sohyun Bang
  5. Heebal Kim
  6. Jae Yong Han  Is a corresponding author
  1. Seoul National University, Korea (South), Republic of
  2. Harvard Medical School, United States
  3. C&K Genomics, Korea (South), Republic of

Abstract

The first-wave of transcriptional activation occurs after fertilisation in species-specific patterns. Despite its importance to initial embryonic development, the characteristics of transcription following fertilisation are poorly understood in Aves. Herein, we report detailed insights into the onset of genome activation in chickens. We established that two waves of transcriptional activation occurred after fertilisation and at Eyal-Giladi and Kochav Stage V. We found 1,544 single-nucleotide polymorphisms across 424 transcripts derived from parents in offspring during the early embryonic stages. Surprisingly, only the maternal genome was activated in the zygote, and the paternal genome remained silent until the second-wave, regardless of the presence of a paternal pronucleus or supernumerary sperm in the egg. The identified maternal genes involved in cleavage were replaced by bi-allelic expression. The results demonstrate that only maternal alleles are activated in the chicken zygote upon fertilisation, which could be essential for early embryogenesis and evolutionary outcomes in birds.

Data availability

Generated WGS of parental chickens has been deposited in BioProject under accession number PRJNA393895 (https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA393895). Generated single hybrid embryonic WTS data has been deposited in GEO under accession number GSE100798 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE100798). Published bulked embryonic WTS data are available under accession number GSE86592 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE86592).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Young Sun Hwang

    Department of Agricultural Biotechnology, Seoul National University, Seoul, Korea (South), Republic of
    Competing interests
    The authors declare that no competing interests exist.
  2. Minseok Seo

    Brigham and Women's Hospital, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5364-7524
  3. Sang Kyung Kim

    Department of Agricultural Biotechnology, Seoul National University, Seoul, Korea (South), Republic of
    Competing interests
    The authors declare that no competing interests exist.
  4. Sohyun Bang

    C&K Genomics, Seoul, Korea (South), Republic of
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2058-1079
  5. Heebal Kim

    Department of Agricultural Biotechnology, Seoul National University, Seoul, Korea (South), Republic of
    Competing interests
    The authors declare that no competing interests exist.
  6. Jae Yong Han

    Department of Agricultural Biotechnology, Seoul National University, Seoul, Korea (South), Republic of
    For correspondence
    jaehan@snu.ac.kr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3413-3277

Funding

National Research Foundation of Korea (NRF-2015R1A3A2033826)

  • Jae Yong Han

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: The experimental use of chickens was approved by the Institute of Laboratory Animal Resources, Seoul National University (SNU-150827-1). The experimental animals were cared for according to a standard management program at the University Animal Farm, Seoul National University, Korea. The procedures for animal management, reproduction and embryo manipulation adhered to the standard operating protocols of our laboratory.

Reviewing Editor

  1. Claudio D Stern, University College London, United Kingdom

Publication history

  1. Received: June 20, 2018
  2. Accepted: October 29, 2018
  3. Accepted Manuscript published: October 30, 2018 (version 1)
  4. Version of Record published: November 19, 2018 (version 2)
  5. Version of Record updated: November 20, 2018 (version 3)

Copyright

© 2018, Hwang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Young Sun Hwang
  2. Minseok Seo
  3. Sang Kyung Kim
  4. Sohyun Bang
  5. Heebal Kim
  6. Jae Yong Han
(2018)
Zygotic gene activation in the chicken occurs in two waves, the first involving only maternally derived genes
eLife 7:e39381.
https://doi.org/10.7554/eLife.39381

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