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Transcriptome sequencing reveals genetic mechanisms underlying the transition between the laying and brooding phases and gene expression changes associated with divergent reproductive phenotypes in chickens

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Abstract

Transition from laying to incubation behavior in chicken is an interesting topic in reproductive biology. The decline of incubation behavior in chicken population has led to considerable phenotypic differences in reproductive traits between breeds. However, the exact genetic mechanism of the reproductive phase transition still largely unknown and little is known about the gene expression changes that contribute to the phenotypic differences. We performed mRNA sequencing to investigate the molecular mechanism underlying the transition from laying to brooding and to detect difference in gene regulation underlying the phenotypic diversification using two chicken breeds. The majority of gene expression changes during phase transition were steroidogenesis and hormone-releasing genes. Brooding chickens shared a conservative pattern of greatly inhibited steroidogenic enzyme genes in the pituitary gland, therefore, low levels of steroidogenic enzymes might result in reproductive defects such as ovary regression and brooding onset. The conserved network responsible for brooding behavior was maintained by steroid biosynthesis and hormonal interactions. Interestingly, three transcription factors, SREBF2, NR5A1 and PGR, act as central signal modulators of steroid biosynthesis and hormonal interactions during the transition from laying to brooding modes at the molecular level. Furthermore, Genes correlated with protein synthesis and accumulation showed expression variation between breeds, which might result in different concentrations of and sensitivities to reproduction-related hormones. This study provided a new insight in neuroendocrine system at the molecular level, and helps to understand the genetic and hormonal responses that ultimately translate into behavior in chicken.

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Acknowledgments

We thank Weiwei Zhai, Jue Ruan, Yu Wang, Gong Qiang and Juan Li of the Beijing Institute of Genomics, Chinese Academy of Science, for important comments on the data analysis. We thank the Guangfeng Baier Huang Breeding Farm, Shangrao city, Jiangxi province, China, for providing BEH chickens. We also thank Liyan Jiang, Hua Zeng and Weimin Li for collecting the XH chicken tissues and Dr. Hongli Du for beneficial discussions and useful advice.

Funding

This work was supported by the following grants: China Agriculture Research System (CARS-42-G05), China High-Tech Programs (2013AA102501), National Natural Science Foundation of China (31301010), as well as the China Postdoctoral Science Foundation (2012M520359).

Author contributions

Xu Shen, Xuemei Lu, Qinghua Nie and Xiquan Zhang conceived and designed the experiments. Xu Shen performed the experiments. Xue Bai, Jin Xu and Xu Shen contributed to data analysis. Min Zhou and Haipin Xu helped to collect the chicken samples. Xu Shen and Xiquan Zhang wrote the manuscript.

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  1. Xiquan Zhang

    Present address: Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding and Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou, 510642, Guangdong, People’s Republic of China

Authors and Affiliations

  1. State Key Laboratory of Biocontrol and Key Laboratory of Gene Engineering of Ministry of Education, School of Life Sciences, Sun Yat-Sen University, Guangzhou, 510275, People’s Republic of China

    Xu Shen

  2. Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding and Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou, 510642, Guangdong, People’s Republic of China

    Xu Shen, Haipin Xu & Qinghua Nie

  3. Laboratory of Disease Genomics and Individualized Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, 100101, People’s Republic of China

    Xu Shen, Xue Bai, Jin Xu & Xuemei Lu

  4. Biotechnology Institute, Nanchang Normal University, Nanchang, 330029, Jiangxi, People’s Republic of China

    Min Zhou

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This study was approved by the Animal Care Committee of South China Agricultural University (Guangzhou, China) under approval number SCAU#0016. The animals used in this study were humanely sacrificed as needed to ameliorate their suffering.

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Shen, X., Bai, X., Xu, J. et al. Transcriptome sequencing reveals genetic mechanisms underlying the transition between the laying and brooding phases and gene expression changes associated with divergent reproductive phenotypes in chickens. Mol Biol Rep 43, 977–989 (2016). https://doi.org/10.1007/s11033-016-4033-8

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