Background <p>Precocious puberty in chickens is an important biological trait regulated by the hypothalamic-pituitary–gonadal (HPG) axis. The comb height of roosters is an indicator of precocious puberty in breeding. However, the underlying mechanisms of precocious puberty, particularly in roosters, remain underexplored.</p> Result <p>This study utilized whole-transcriptome sequencing of the hypothalamus, pituitary, and testicle to identify candidate genes and competitive endogenous RNA (ceRNA) networks associated with precocious puberty. The result showed that early sexually mature roosters exhibited more developed testicles and comb, along with elevated levels of gonadotropin -releasing hormone (GnRH), luteinizing hormone (LH), and testosterone. A total of 108 differential expressed genes (DEGs), 18 differential expressed lncRNAs (DElncRNAs), and 54 differential expressed miRNAs (DEmiRNAs) were identified in the hypothalamus; 190 DEGs, 27 DElncRNAs, and 45 DEmiRNAs in the pituitary; and 339 DEGs, 48 DElncRNAs, and 626 DEmiRNAs in the testicle. Notably, <i>NMRK2</i> and <i>PSMD14</i> were co-expressed across these tissues, with higher expression in sexually mature roosters. Furthermore, 13 genes including <i>PCDH9</i>, <i>RAB3C</i>, <i>MYO5A</i>, <i>SYNE2</i>, <i>ATP8B5</i> and <i>EIF4G1</i>, were co-expressed in the hypothalamus and pituitary, while 17 genes including <i>SMG7</i>, <i>PTPRS</i>, <i>C20ORF194</i> and <i>RNF213</i> were co-expressed in the pituitary and testicle. Protein–protein interaction (PPI) network analysis identified key regulatory genes for sexual maturation, including <i>MYO5A</i>, <i>NMRK2</i>, <i>AKT3</i>, <i>CREB1</i>, and <i>EIF4G1</i> in the hypothalamus; <i>ERBB4</i>, <i>MYO5A</i>, <i>PTPRF</i>, and <i>CDK6</i> in the pituitary; and <i>SRC</i>, <i>PSMD14</i>, <i>UBE2O</i>, and <i>PIK3CB</i> in the testicle. The ceRNA network TCONS_00062798/TCONS_0008908—gga-miR-206—<i>AKT3</i> in the hypothalamus regulates GnRH secretion, promoting sexual maturation via ErbB and MAPK signaling pathways. The ceRNA network <i>circ_02349 0</i>-<i>TCONS_00071970</i>- <i>gga-miR-183</i>/<i>gga-miR-200a-3p/novel-m29153p</i>—<i>CDK6</i> of the pituitary may inhibit LH release by disrupting the cell cycle, reducing sexual maturation. In the testicle, the ceRNA network <i>novel_circ_022575</i>/<i>novel_circ_006317</i>/<i>ENSGALT0 0000076697</i>/<i>ENSGALT00000046820</i>—<i>miR-16-x</i>/<i>gga-miR-16c-5p</i>—<i>SRC</i> regulates testosterone secretion through PPAR, TGF-β, and mTOR signaling pathways, indirectly influencing GnRH and gonadotropin release.</p> Conclusion <p>These findings identified candidate genes and ceRNA networks associated with sexual precocity regulation in the HPG axis of the rooster, not only providing novel mechanisms underlying rooster sexual precocity but also highlighting the complex interplay between tissues in the HPG axis.</p>

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Identification of candidate genes and ceRNA networks of HPG axis in regulating sexual precocity of roosters by whole transcriptomic sequencing

  • Hai Xiang,
  • Xiangkun Li,
  • Xiaoxu Sun,
  • Zhengfen Zhang,
  • Jixiang Wei,
  • Zhijie Liu,
  • Zheng Ma,
  • Siyu Chen,
  • Junwei Gou,
  • Fei Ye,
  • Hua Li

摘要

Background

Precocious puberty in chickens is an important biological trait regulated by the hypothalamic-pituitary–gonadal (HPG) axis. The comb height of roosters is an indicator of precocious puberty in breeding. However, the underlying mechanisms of precocious puberty, particularly in roosters, remain underexplored.

Result

This study utilized whole-transcriptome sequencing of the hypothalamus, pituitary, and testicle to identify candidate genes and competitive endogenous RNA (ceRNA) networks associated with precocious puberty. The result showed that early sexually mature roosters exhibited more developed testicles and comb, along with elevated levels of gonadotropin -releasing hormone (GnRH), luteinizing hormone (LH), and testosterone. A total of 108 differential expressed genes (DEGs), 18 differential expressed lncRNAs (DElncRNAs), and 54 differential expressed miRNAs (DEmiRNAs) were identified in the hypothalamus; 190 DEGs, 27 DElncRNAs, and 45 DEmiRNAs in the pituitary; and 339 DEGs, 48 DElncRNAs, and 626 DEmiRNAs in the testicle. Notably, NMRK2 and PSMD14 were co-expressed across these tissues, with higher expression in sexually mature roosters. Furthermore, 13 genes including PCDH9, RAB3C, MYO5A, SYNE2, ATP8B5 and EIF4G1, were co-expressed in the hypothalamus and pituitary, while 17 genes including SMG7, PTPRS, C20ORF194 and RNF213 were co-expressed in the pituitary and testicle. Protein–protein interaction (PPI) network analysis identified key regulatory genes for sexual maturation, including MYO5A, NMRK2, AKT3, CREB1, and EIF4G1 in the hypothalamus; ERBB4, MYO5A, PTPRF, and CDK6 in the pituitary; and SRC, PSMD14, UBE2O, and PIK3CB in the testicle. The ceRNA network TCONS_00062798/TCONS_0008908—gga-miR-206—AKT3 in the hypothalamus regulates GnRH secretion, promoting sexual maturation via ErbB and MAPK signaling pathways. The ceRNA network circ_02349 0-TCONS_00071970- gga-miR-183/gga-miR-200a-3p/novel-m29153pCDK6 of the pituitary may inhibit LH release by disrupting the cell cycle, reducing sexual maturation. In the testicle, the ceRNA network novel_circ_022575/novel_circ_006317/ENSGALT0 0000076697/ENSGALT00000046820miR-16-x/gga-miR-16c-5pSRC regulates testosterone secretion through PPAR, TGF-β, and mTOR signaling pathways, indirectly influencing GnRH and gonadotropin release.

Conclusion

These findings identified candidate genes and ceRNA networks associated with sexual precocity regulation in the HPG axis of the rooster, not only providing novel mechanisms underlying rooster sexual precocity but also highlighting the complex interplay between tissues in the HPG axis.