Zygotic gene activation in the chicken occurs in two waves, the first involving only maternally derived genes
- Seoul National University, Korea (South), Republic of
- Harvard Medical School, United States
- 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).
Article and author information
Author details
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.
Reviewing Editor
- Claudio D Stern, University College London, United Kingdom
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.
Version history
- Received: June 20, 2018
- Accepted: October 29, 2018
- Accepted Manuscript published: October 30, 2018 (version 1)
- Version of Record published: November 19, 2018 (version 2)
- 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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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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A crucial event in sexual reproduction is when haploid sperm and egg fuse to form a new diploid organism at fertilization. In mammals, direct interaction between egg JUNO and sperm IZUMO1 mediates gamete membrane adhesion, yet their role in fusion remains enigmatic. We used AlphaFold to predict the structure of other extracellular proteins essential for fertilization to determine if they could form a complex that may mediate fusion. We first identified TMEM81, whose gene is expressed by mouse and human spermatids, as a protein having structural homologies with both IZUMO1 and another sperm molecule essential for gamete fusion, SPACA6. Using a set of proteins known to be important for fertilization and TMEM81, we then systematically searched for predicted binary interactions using an unguided approach and identified a pentameric complex involving sperm IZUMO1, SPACA6, TMEM81 and egg JUNO, CD9. This complex is structurally consistent with both the expected topology on opposing gamete membranes and the location of predicted N-glycans not modeled by AlphaFold-Multimer, suggesting that its components could organize into a synapse-like assembly at the point of fusion. Finally, the structural modeling approach described here could be more generally useful to gain insights into transient protein complexes difficult to detect experimentally.
