The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers

Layer and broiler hens show a dramatic difference in the volume and frequency of egg production. However, it is unclear whether the intrinsic competency of oocyte generation is also different between the two types of chicken. All oocytes were derived from the primordial germ cells (PGC) in the devel...

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Main Authors: Yuxiao Ma, Wenhui Wu, Yun Zhang, Xuzhao Wang, Jiahui Wei, Xiaotong Guo, Man Xue, Guiyu Zhu
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/14/4/781
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author Yuxiao Ma
Wenhui Wu
Yun Zhang
Xuzhao Wang
Jiahui Wei
Xiaotong Guo
Man Xue
Guiyu Zhu
author_facet Yuxiao Ma
Wenhui Wu
Yun Zhang
Xuzhao Wang
Jiahui Wei
Xiaotong Guo
Man Xue
Guiyu Zhu
author_sort Yuxiao Ma
collection DOAJ
description Layer and broiler hens show a dramatic difference in the volume and frequency of egg production. However, it is unclear whether the intrinsic competency of oocyte generation is also different between the two types of chicken. All oocytes were derived from the primordial germ cells (PGC) in the developing embryo, and female PGC proliferation (mitosis) and the subsequent differentiation (meiosis) determine the ultimate ovarian pool of germ cells available for future ovulation. In this study, we systematically compared the cellular phenotype and gene expression patterns during PGC mitosis (embryonic day 10, E10) and meiosis (E14) between female layers and broilers to determine whether the early germ cell development is also subjected to the selective breeding of egg production traits. We found that PGCs from E10 showed much higher activity in cell propagation and were enriched in cell proliferation signaling pathways than PGCs from E14 in both types of chicken. A common set of genes, namely insulin-like growth factor 2 (<i>IGF2</i>) and E2F transcription factor 4 (<i>E2F4</i>), were identified as the major regulators of cell proliferation in E10 PGCs of both strains. In addition, we found that E14 PGCs from both strains showed an equal ability to initiate meiosis, which was associated with the upregulation of key genes for meiotic initiation. The intrinsic cellular dynamics during the transition from proliferation to differentiation of female germ cells were conserved between layers and broilers. Hence, we surmise that other non-cell autonomous mechanisms involved in germ-somatic cell interactions would contribute to the divergence of egg production performance between layers and broilers.
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spelling doaj.art-fb7e3625f02542d185a9ec00e6b9b0bf2023-11-17T19:22:20ZengMDPI AGGenes2073-44252023-03-0114478110.3390/genes14040781The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and BroilersYuxiao Ma0Wenhui Wu1Yun Zhang2Xuzhao Wang3Jiahui Wei4Xiaotong Guo5Man Xue6Guiyu Zhu7Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, Tai’an 271000, ChinaShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, Tai’an 271000, ChinaShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, Tai’an 271000, ChinaShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, Tai’an 271000, ChinaShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, Tai’an 271000, ChinaShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, Tai’an 271000, ChinaShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, Tai’an 271000, ChinaShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University, Tai’an 271000, ChinaLayer and broiler hens show a dramatic difference in the volume and frequency of egg production. However, it is unclear whether the intrinsic competency of oocyte generation is also different between the two types of chicken. All oocytes were derived from the primordial germ cells (PGC) in the developing embryo, and female PGC proliferation (mitosis) and the subsequent differentiation (meiosis) determine the ultimate ovarian pool of germ cells available for future ovulation. In this study, we systematically compared the cellular phenotype and gene expression patterns during PGC mitosis (embryonic day 10, E10) and meiosis (E14) between female layers and broilers to determine whether the early germ cell development is also subjected to the selective breeding of egg production traits. We found that PGCs from E10 showed much higher activity in cell propagation and were enriched in cell proliferation signaling pathways than PGCs from E14 in both types of chicken. A common set of genes, namely insulin-like growth factor 2 (<i>IGF2</i>) and E2F transcription factor 4 (<i>E2F4</i>), were identified as the major regulators of cell proliferation in E10 PGCs of both strains. In addition, we found that E14 PGCs from both strains showed an equal ability to initiate meiosis, which was associated with the upregulation of key genes for meiotic initiation. The intrinsic cellular dynamics during the transition from proliferation to differentiation of female germ cells were conserved between layers and broilers. Hence, we surmise that other non-cell autonomous mechanisms involved in germ-somatic cell interactions would contribute to the divergence of egg production performance between layers and broilers.https://www.mdpi.com/2073-4425/14/4/781chickenprimordial germ cellsproliferationmitosismeiosis
spellingShingle Yuxiao Ma
Wenhui Wu
Yun Zhang
Xuzhao Wang
Jiahui Wei
Xiaotong Guo
Man Xue
Guiyu Zhu
The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers
Genes
chicken
primordial germ cells
proliferation
mitosis
meiosis
title The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers
title_full The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers
title_fullStr The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers
title_full_unstemmed The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers
title_short The Synchronized Progression from Mitosis to Meiosis in Female Primordial Germ Cells between Layers and Broilers
title_sort synchronized progression from mitosis to meiosis in female primordial germ cells between layers and broilers
topic chicken
primordial germ cells
proliferation
mitosis
meiosis
url https://www.mdpi.com/2073-4425/14/4/781
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