与鸡性成熟及其杂种优势相关的全基因组circRNA信号分析

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (2): 697-711.DOI: 10.1016/j.jia.2023.05.026

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与鸡性成熟及其杂种优势相关的全基因组circRNA信号分析

收稿日期:2023-01-19 接受日期:2023-04-17 出版日期:2025-02-20 发布日期:2025-01-22

Genome-wide circular RNAs signatures involved in sexual maturation and its heterosis in chicken

Yuanmei Wang^*, Jingwei Yuan^*, Yanyan Sun, Aixin Ni, Jinmeng Zhao, Yunlei Li, Panlin Wang, Lei Shi, Yunhe Zong, Pingzhuang Ge, Shixiong Bian, Hui Ma, Jilan Chen^#

State Key Laboratory of Animal Biotech Breeding, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Received:2023-01-19 Accepted:2023-04-17 Online:2025-02-20 Published:2025-01-22
About author:Yuanmei Wang, E-mail: ymwang062723@163.com; Jingwei Yuan, E-mail: yuanjingwei@caas.cn; #Correspondence Jilan Chen, E-mail: Chen.jilan@163.com * These authors contribute equally to this study.
Supported by:
This research was funded by the National Natural Science Foundation of China (32172721), China Agriculture Research System (CARS-40), Central Public-interest Scientific Institution Basal Research Fund (2021-YWF-ZYSQ-12) and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences (ASTIP-IAS04).

摘要/Abstract

摘要：

性成熟杂种优势已在动物杂交育种中广泛使用，但鸡性成熟杂种优势分子机理尚未揭示清楚。本研究以白来航鸡和北京油鸡为亲本构建完全双列杂交群体，测定纯繁（WW，YY）和正反交（WY，YW）组合四个群体性成熟相关性状。通过分析纯繁和正反交组合卵巢circRNA表达谱解析性成熟杂种优势潜在的分子机理。研究发现正反交组合耻骨间距、输卵管长度和见蛋日龄均表现为杂种优势。我们在四个组合卵巢中共鉴定到3,649个circRNA，其中包括3,025个已知circRNAs和624个新circRNAs，这些circRNA主要为外显子类型。WY和YW组合中特异性表达circRNAs分别为141和178个。通过对鉴定circRNAs进行差异分析和表达模式分析，发现WY和YW组合中非加性表达circRNAs分别占其总鉴定circRNA的52.38%和64.63%。GO和KEGG功能富集分析结果显示非加性效应circRNAs来源基因主要参与TGF-beta信号通路，卵母细胞生长发育，ATP酶激活活性，卵母细胞有丝分裂，孕酮调控卵母细胞成熟和GnRH信号通路等。通过加权共表达网络分析共鉴定到四个模块与输卵管长度和耻骨间距显著相关。这四个模块中的非加性表达circRNAs主要参与MAPK信号通路和Wnt信号通路。我们进一步对非加性circRNA进行竞争性内源RNA（ceRNA）网络分析，鉴定到gall-FGFR2_0005和gal-MAPKAP1_0004可与miRNA gga-miR-1612和gga-miR-12235-5p竞争性结合进而调控基因CNOT6，COL8A1和FHL2的非加性表达，参与卵巢的发育过程。以上结果表明非加性效应circRNAs可通过调控繁殖和发育过程相关基因促进性成熟杂种优势的形成。该研究首次从circRNA水平揭示了鸡性成熟杂种优势形成的潜在分子机理，为丰富畜禽杂种优势分子机理探究及杂种优势科学应用提供了理论基础。

Abstract:

Sexual maturation heterosis has been widely exploited in animal crossbreeding. However, the underlying mechanism has been rarely explored in chicken. In the present study, we performed the reciprocal crossing between White Leghorn and Beijing You chicken to evaluate the phenotypes related to sexual maturation, and profiled the ovary circRNAs of purebreds (WW, YY) and crossbreds (WY, YW) to elucidate the molecular mechanism underlying heterosis for sexual maturation. Pubic space and oviduct length exhibited positive heterosis, and age at first egg (AFE) exhibited negative heterosis in the crossbreds. We identified 3,025 known circRNAs and 624 putative circRNAs, which were mainly derived from the exons. Among these circRNAs, 141 and 178 circRNAs were specially expressed in WY and YW, respectively. There were 52.38 and 64.63% of total circRNAs in WY and YW exhibited non-additive expression pattern, respectively. GO enrichment and KEGG pathway analysis showed that the host genes of non-additive circRNAs were mainly involved in TGF-beta signaling pathway, oocyte development, ATPase activator activity, oocyte meiosis, progesterone-mediated oocyte maturation and GnRH signaling pathway. Weighted gene co-expression network analysis identified that 4 modules were significantly (P<0.05) correlated with oviduct length and pubic space. The host genes of non-additive circRNAs harbored in the 4 modules were associated with MAPK signaling pathway and Wnt signaling pathway. Furthermore, competing endogenous RNAs (ceRNA) network analysis characterized non-additive circRNAs gal-FGFR2_0005 and gal-MAPKAP1_0004 could interact with gga-miR-1612 and gga-miR-12235-5p to regulate CNOT6, COL8A1, and FHL2, which were essential for ovary development, indicating that the non-additive circRNAs involved in the formation of sexual maturation heterosis through regulating genes related to the reproductive and developmental process. The findings would provide a deeper understanding of the molecular mechanism underlying sexual maturation heterosis from a novel perspective.

Key words: chicken , sexual maturation , heterosis , ovary , circRNA

Yuanmei Wang, Jingwei Yuan, Yanyan Sun, Aixin Ni, Jinmeng Zhao, Yunlei Li, Panlin Wang, Lei Shi, Yunhe Zong, Pingzhuang Ge, Shixiong Bian, Hui Ma, Jilan Chen. 与鸡性成熟及其杂种优势相关的全基因组circRNA信号分析[J]. Journal of Integrative Agriculture, 2025, 24(2): 697-711.

Yuanmei Wang, Jingwei Yuan, Yanyan Sun, Aixin Ni, Jinmeng Zhao, Yunlei Li, Panlin Wang, Lei Shi, Yunhe Zong, Pingzhuang Ge, Shixiong Bian, Hui Ma, Jilan Chen. Genome-wide circular RNAs signatures involved in sexual maturation and its heterosis in chicken[J]. Journal of Integrative Agriculture, 2025, 24(2): 697-711.

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