Regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chicken

Abstract Background Crossbreeding is widely promoted as an efficient strategy to improve the productivity in agriculture. The molecular mechanism underlying heterosis for egg production is always intriguing in chicken. The transcriptional dynamic changes play a crucial role in the formation of heter...

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Main Authors: Jingwei Yuan, Yuanmei Wang, Yanyan Sun, Yunlei Li, Aixin Ni, Qin Li, Hanhan Yang, Xinying Xu, Yunhe Zong, Hui Ma, Jilan Chen
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Journal of Animal Science and Biotechnology
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Online Access:https://doi.org/10.1186/s40104-025-01156-2
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author Jingwei Yuan
Yuanmei Wang
Yanyan Sun
Yunlei Li
Aixin Ni
Qin Li
Hanhan Yang
Xinying Xu
Yunhe Zong
Hui Ma
Jilan Chen
author_facet Jingwei Yuan
Yuanmei Wang
Yanyan Sun
Yunlei Li
Aixin Ni
Qin Li
Hanhan Yang
Xinying Xu
Yunhe Zong
Hui Ma
Jilan Chen
author_sort Jingwei Yuan
collection DOAJ
description Abstract Background Crossbreeding is widely promoted as an efficient strategy to improve the productivity in agriculture. The molecular mechanism underlying heterosis for egg production is always intriguing in chicken. The transcriptional dynamic changes play a crucial role in the formation of heterosis, but little is known for the egg production traits. Results In present study, we measured the continuous manifestation of heterosis ranging from 2.67% to 10.24% for egg number in the crossbreds generated by reciprocal crossing White Leghorn and Beijing You chicken. The high-quality transcriptomes of ovary for purebreds (WW and YY) and crossbreds (WY and YW) in 5 laying stages were sequenced and integrated to identify regulatory networks relevant to the heterosis. We found highly conserved transcriptional features among 4 genetic groups. By using weighted gene co-expression network analysis (WGCNA), we obtained multiple gene co-expression modules that were significantly correlated with egg number for each group. The common KEGG pathways including apelin signaling pathway, cell cycle, ribosome, spliceosome and oxidative phosphorylation, were screened for the 2 crossbreds. Then, we identified consensus co-expression modules (CMs) that showed divergent expression pattern among crossbred (WY or YW) and purebreds (WW and YY). The hub genes of CMs were again overrepresented in the cell cycle pathway, and the crossbreds exhibited temporally complementary dominance of hub genes in the 5 laying stages. These results suggested that the crossbreds inherited from both parents to maintain the ovary function by cell cycle-related genes, contributing to the persistent heterosis for egg production. Furthermore, the dominant genes including MAD2L1, CHEK2 and E2F1 were demonstrated to function in ovarian follicle development and maturation and could be the candidate genes for egg production heterosis. Conclusion Our study characterized the dynamic profile of genome-wide gene expression in ovary and highlighted the role of dominant expression of cell cycle pathway genes in heterosis. These findings provided new insights for the molecular mechanism of egg production heterosis, which would facilitate the rational choice of suitable parents for producing crossbred chickens with higher egg production.
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spelling doaj-art-24c58e1f9375403d826f2e6475ba80952025-02-09T12:49:09ZengBMCJournal of Animal Science and Biotechnology2049-18912025-02-0116111410.1186/s40104-025-01156-2Regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chickenJingwei Yuan0Yuanmei Wang1Yanyan Sun2Yunlei Li3Aixin Ni4Qin Li5Hanhan Yang6Xinying Xu7Yunhe Zong8Hui Ma9Jilan Chen10Key Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural UniversityKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural SciencesAbstract Background Crossbreeding is widely promoted as an efficient strategy to improve the productivity in agriculture. The molecular mechanism underlying heterosis for egg production is always intriguing in chicken. The transcriptional dynamic changes play a crucial role in the formation of heterosis, but little is known for the egg production traits. Results In present study, we measured the continuous manifestation of heterosis ranging from 2.67% to 10.24% for egg number in the crossbreds generated by reciprocal crossing White Leghorn and Beijing You chicken. The high-quality transcriptomes of ovary for purebreds (WW and YY) and crossbreds (WY and YW) in 5 laying stages were sequenced and integrated to identify regulatory networks relevant to the heterosis. We found highly conserved transcriptional features among 4 genetic groups. By using weighted gene co-expression network analysis (WGCNA), we obtained multiple gene co-expression modules that were significantly correlated with egg number for each group. The common KEGG pathways including apelin signaling pathway, cell cycle, ribosome, spliceosome and oxidative phosphorylation, were screened for the 2 crossbreds. Then, we identified consensus co-expression modules (CMs) that showed divergent expression pattern among crossbred (WY or YW) and purebreds (WW and YY). The hub genes of CMs were again overrepresented in the cell cycle pathway, and the crossbreds exhibited temporally complementary dominance of hub genes in the 5 laying stages. These results suggested that the crossbreds inherited from both parents to maintain the ovary function by cell cycle-related genes, contributing to the persistent heterosis for egg production. Furthermore, the dominant genes including MAD2L1, CHEK2 and E2F1 were demonstrated to function in ovarian follicle development and maturation and could be the candidate genes for egg production heterosis. Conclusion Our study characterized the dynamic profile of genome-wide gene expression in ovary and highlighted the role of dominant expression of cell cycle pathway genes in heterosis. These findings provided new insights for the molecular mechanism of egg production heterosis, which would facilitate the rational choice of suitable parents for producing crossbred chickens with higher egg production.https://doi.org/10.1186/s40104-025-01156-2Cell cycleChickenDominanceEgg production heterosisOvary transcriptomeWGCNA
spellingShingle Jingwei Yuan
Yuanmei Wang
Yanyan Sun
Yunlei Li
Aixin Ni
Qin Li
Hanhan Yang
Xinying Xu
Yunhe Zong
Hui Ma
Jilan Chen
Regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chicken
Journal of Animal Science and Biotechnology
Cell cycle
Chicken
Dominance
Egg production heterosis
Ovary transcriptome
WGCNA
title Regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chicken
title_full Regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chicken
title_fullStr Regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chicken
title_full_unstemmed Regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chicken
title_short Regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chicken
title_sort regulatory signatures involved in the cell cycle pathway contribute to egg production heterosis in chicken
topic Cell cycle
Chicken
Dominance
Egg production heterosis
Ovary transcriptome
WGCNA
url https://doi.org/10.1186/s40104-025-01156-2
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