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.

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.

Metrics

  • 2,663
    views
  • 384
    downloads
  • 15
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.39381

Further reading

    1. Developmental Biology
    Saira Amir, Olatunbosun Arowolo ... Alexander Suvorov
    Research Article

    Over the past several decades, a trend toward delayed childbirth has led to increases in parental age at the time of conception. Sperm epigenome undergoes age-dependent changes increasing risks of adverse conditions in offspring conceived by fathers of advanced age. The mechanism(s) linking paternal age with epigenetic changes in sperm remain unknown. The sperm epigenome is shaped in a compartment protected by the blood-testes barrier (BTB) known to deteriorate with age. Permeability of the BTB is regulated by the balance of two mTOR complexes in Sertoli cells where mTOR complex 1 (mTORC1) promotes the opening of the BTB and mTOR complex 2 (mTORC2) promotes its integrity. We hypothesized that this balance is also responsible for age-dependent changes in the sperm epigenome. To test this hypothesis, we analyzed reproductive outcomes, including sperm DNA methylation in transgenic mice with Sertoli cell-specific suppression of mTORC1 (Rptor KO) or mTORC2 (Rictor KO). mTORC2 suppression accelerated aging of the sperm DNA methylome and resulted in a reproductive phenotype concordant with older age, including decreased testes weight and sperm counts, and increased percent of morphologically abnormal spermatozoa and mitochondrial DNA copy number. Suppression of mTORC1 resulted in the shift of DNA methylome in sperm opposite to the shift associated with physiological aging – sperm DNA methylome rejuvenation and mild changes in sperm parameters. These results demonstrate for the first time that the balance of mTOR complexes in Sertoli cells regulates the rate of sperm epigenetic aging. Thus, mTOR pathway in Sertoli cells may be used as a novel target of therapeutic interventions to rejuvenate the sperm epigenome in advanced-age fathers.

    1. Developmental Biology
    Jing Wang, Yingying Yin ... Zhaojian Liu
    Research Article

    Transmembrane channel-like (TMC) proteins are a highly conserved ion channel family consisting of eight members (TMC1–TMC8) in mammals. TMC1/2 are components of the mechanotransduction channel in hair cells, and mutations of TMC1/2 cause deafness in humans and mice. However, the physiological roles of other TMC proteins remain largely unknown. Here, we show that Tmc7 is specifically expressed in the testis and that it is required for acrosome biogenesis during spermatogenesis. Tmc7−/− mice exhibited abnormal sperm head, disorganized mitochondrial sheaths, and reduced number of elongating spermatids, similar to human oligo-astheno-teratozoospermia. We further demonstrate that TMC7 is colocalized with GM130 at the cis-Golgi region in round spermatids. TMC7 deficiency leads to aberrant Golgi morphology and impaired fusion of Golgi-derived vesicles to the developing acrosome. Moreover, upon loss of TMC7 intracellular ion homeostasis is impaired and ROS levels are increased, which in turn causes Golgi and endoplasmic reticulum stress. Taken together, these results suggest that TMC7 is required to maintain pH and ion homeostasis, which is needed for acrosome biogenesis. Our findings unveil a novel role for TMC7 in acrosome biogenesis during spermiogenesis.