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

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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

1. Han J
2. Hwang Y
(2018) Avian zygote activates only maternal allele to disburden high variation of supernumerary sperms contrary to mammal
NCBI Gene Expression Omnibus, GSE100798.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE100798
1. Han J
2. Hwang Y
(2018) Avian zygote activates only maternal allele to disburden high variation of supernumerary sperms contrary to mammal
NCBI BioProject, PRJNA393895.

https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA393895

The following previously published data sets were used

1. Hwang YS
2. Seo M
3. Bang S
4. Kim H
5. Han JY
(2018) Transcriptional and translational dynamics during maternal-to-zygotic transition in early chicken development
NCBI Gene Expression Omnibus, GSE86592.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE86592
1. Hwang YS
2. Seo M
3. Lee BR
4. Lee HJ
5. Park YH
6. Kim SK
7. Lee HC
8. Choi HJ
9. Yoon J
10. Kim H
11. Han JY
(2018) The transcriptome of early chicken embryos reveals signaling pathways governing rapid asymmetric cellularization and lineage segregation
NCBI Gene Expression Omnibus, GSE86592.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE86592

Article and author information

Author details

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.
Minseok Seo

Brigham and Women's Hospital, Harvard Medical School, Boston, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5364-7524
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.
Sohyun Bang

C&K Genomics, Seoul, Korea (South), Republic of

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2058-1079
Heebal Kim

Department of Agricultural Biotechnology, Seoul National University, Seoul, Korea (South), Republic of

Competing interests
The authors declare that no competing interests exist.
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.

"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

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.