{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,15]],"date-time":"2026-09-15T18:04:15Z","timestamp":1789495455788,"version":"build-2803163510"},"reference-count":35,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,10,16]],"date-time":"2025-10-16T00:00:00Z","timestamp":1760572800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Genet."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>The long egg-laying interval of pigeons leads to low egg production, and the hypothalamus-pituitary-ovary (HPO) axis plays a crucial role in regulating the egg-laying process of poultry. European meat pigeons have a shorter egg-laying interval than Shiqi pigeons, but the molecular mechanism underlying this difference remains unclear.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Reproductive phenotypic data of 300 pairs of pigeons from each breed were collected for 6 months. Five 2-2.5-year-old female pigeons from each breed were selected, and their hypothalamus, pituitary, and ovary tissues were collected for transcriptome sequencing. Differentially Expressed Genes (DEGs) were identified, and Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses were performed.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>The egg-laying interval of European meat pigeons (32.76 \u00b1 3.25 days) was significantly shorter than that of Shiqi pigeons (33.11 \u00b1 3.86 days, P=0.024). A total of 39, 101, and 199 DEGs were identified in the comparisons of SH vs EH, SP vs EP, and SO vs EO, respectively. DEGs in the hypothalamus and pituitary were enriched in pathways such as thyroid hormone transport and calcium-mediated signaling; DEGs in the ovary were enriched in pathways such as embryonic development and steroid biosynthesis. The thyroid hormone signaling pathway (in the hypothalamus and pituitary) and the steroid hormone biosynthesis pathway (in the ovary) were significantly enriched, and key genes such as StAR, EYA1, HAND2, HOXB8, and NRN1 were identified.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>The hypothalamus-pituitary-ovary axis regulates the egg-laying interval of pigeons through tissue-specific pathways. Among them, the thyroid hormone signaling pathway controls upstream hormone secretion, and the steroid biosynthesis pathway affects follicle maturation. The identified key genes may serve as targets for shortening the egg-laying interval.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fgene.2025.1676255","type":"journal-article","created":{"date-parts":[[2025,10,16]],"date-time":"2025-10-16T03:51:33Z","timestamp":1760586693000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":3,"title":["Transcriptome profiling of hypothalamus-pituitary-ovary axis provides insights into egg-laying interval differences between european meat pigeons and shiqi pigeons"],"prefix":"10.3389","volume":"16","author":[{"given":"Xinlei","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liyu","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruiting","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liheng","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhanbing","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Runzhi","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiang","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dingding","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mingjun","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pengkun","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,10,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1016\/j.mcn.2018.01.008","article-title":"Reproductive role of miRNA in the hypothalamic-pituitary axis","volume":"88","author":"Chunyu","year":"2018","journal-title":"Mol. Cell. Neurosci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.mce.2016.07.036","article-title":"A brief history of the search for the protein(s) involved in the acute regulation of steroidogenesis","volume":"441","author":"Douglas","year":"2017","journal-title":"Mol. Cell. Endocrinol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1677\/joe.0.0910011","article-title":"Changes in the plasma concentrations of luteinizing hormone, progesterone, oestradiol and testosterone and in the binding of follicle-stimulating hormone to the theca of follicles during the ovulation cycle of the hen (Gallus domesticus)","volume":"91","author":"Etches","year":"1981","journal-title":"J. Endocrinol."},{"key":"B4","doi-asserted-by":"crossref","DOI":"10.1101\/2021.12.13.472470","volume-title":"Prolactin maintains parental responses and alters reproductive axis gene expression, but not courtship behaviors, in both sexes of a biparental bird","author":"Farrar","year":"2021"},{"key":"B5","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1006\/dbio.2001.0417","article-title":"The combinatorial activities of Nkx2.5 and dHAND are essential for cardiac ventricle formation","volume":"239","author":"Hiroyuki","year":"2001","journal-title":"Dev. Biol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1016\/j.ygcen.2014.12.022","article-title":"Growth hormone production and role in the reproductive system of female chicken","volume":"220","author":"Hrabia","year":"2015","journal-title":"Gen. Comp. Endocrinol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1007\/s00441-011-1187-5","article-title":"Effect of growth hormone on steroid content, proliferation and apoptosis in the chicken ovary during sexual maturation","volume":"345","author":"Hrabia","year":"2011","journal-title":"Cell Tissue Res."},{"key":"B8","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.domaniend.2017.05.002","article-title":"Effects of nonglycosylated and glycosylated prolactin on basal and gonadotropin-stimulated steroidogenesis in chicken ovarian follicles","volume":"61","author":"Hu","year":"2017","journal-title":"Domest. Anim. Endocrinol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"660","DOI":"10.3906\/vet-1405-6","article-title":"The avian ovary and follicle development: some comparative and practical insights","volume":"38","author":"Johnson","year":"2014","journal-title":"Turkish J. Veterinary Animal Sci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"113446","DOI":"10.1016\/j.ygcen.2020.113446","article-title":"The hypothalamic-pituitary-gonadal axis and thyroid hormone regulation interact to influence seasonal breeding in green anole lizards (Anolis carolinensis)","volume":"292","author":"Kang","year":"2020","journal-title":"Gen. Comp. Endocrinol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"7041","DOI":"10.3382\/ps\/pez437","article-title":"Characterization of gene expression in the hypothalamo-pituitary-gonadal axis during the preovulatory surge in the Turkey hen","volume":"98","author":"Kristen","year":"2019","journal-title":"Poult. Sci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0739-7240(97)00057-X","article-title":"Two steroidogenic pathways present in the chicken ovary: theca layer prefers \u03945 pathway and granulosa layer prefers \u03944 pathway","volume":"15","author":"Lee","year":"1998","journal-title":"Domest. Anim. Endocrinol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"668","DOI":"10.1002\/jcp.20598","article-title":"Heterogeneity of the Ca2+ sensitivity of secretion in a pituitary gonadotrope cell line and its modulation by protein kinase C and Ca2+","volume":"207","author":"Liu","year":"2006","journal-title":"J. Cell Physiol."},{"key":"B14","first-page":"447","article-title":"Nutritional analysis and evaluation of pigeon meat","volume":"32","author":"Long","year":"2011","journal-title":"Food industry Sci. Technol."},{"key":"B15","first-page":"109","article-title":"Pigeons as laboratory animals","volume":"10","author":"Nepote","year":"1999","journal-title":"Avian and Poult. Biol. Rev."},{"key":"B16","doi-asserted-by":"publisher","first-page":"12735","DOI":"10.3390\/ijms222312735","article-title":"The roles of luteinizing hormone, follicle-stimulating hormone and testosterone in spermatogenesis and folliculogenesis revisited","volume":"22","author":"Oduwole","year":"2021","journal-title":"Int. J. Mol. Sci."},{"key":"B17","doi-asserted-by":"publisher","first-page":"2890","DOI":"10.14202\/vetworld.2022.2890-2895","article-title":"Effect of follicle-stimulating hormone and luteinizing hormone levels on egg-laying frequency in hens","volume":"15","author":"Prastiya","year":"2022","journal-title":"Vet. World"},{"key":"B18","doi-asserted-by":"publisher","first-page":"602","DOI":"10.1016\/j.ydbio.2006.08.059","article-title":"Eya1 and Eya2 proteins are required for hypaxial somitic myogenesis in the mouse embryo","volume":"302","author":"Raphaelle","year":"2007","journal-title":"Dev. Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"2708","DOI":"10.3390\/ijms23052708","article-title":"A new perspective on thyroid hormones: crosstalk with reproductive hormones in females","volume":"23","author":"Ren","year":"2022","journal-title":"Int. J. Mol. Sci."},{"key":"B20","doi-asserted-by":"publisher","first-page":"36637","DOI":"10.1074\/jbc.M006456200","article-title":"Lipoproteins regulate expression of the steroidogenic acute regulatory protein (StAR) in mouse adrenocortical cells","volume":"275","author":"Reyland","year":"2000","journal-title":"J. Biol. Chem."},{"key":"B21","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.ygcen.2013.04.012","article-title":"The role of thyroid hormones in regulation of chicken ovarian steroidogenesis","volume":"190","author":"Sechman","year":"2013","journal-title":"General Comp. Endocrinol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.toxlet.2016.11.001","article-title":"Effects of PCB 126 and PCB 153 on secretion of steroid hormones and mRNA expression of steroidogenic genes (STAR, HSD3B, CYP19A1) and estrogen receptors (ER\u03b1, ER\u03b2) in prehierarchical chicken ovarian follicles","volume":"264","author":"Sechman","year":"2016","journal-title":"Toxicol. Lett."},{"key":"B23","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/S0074-7696(08)60836-0","article-title":"Immunocytochemistry of the Avian hypothalamus and adenohypophysis","volume":"103","author":"Shin-ichi","year":"1986","journal-title":"Int. Rev. Cytol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1093\/biolre\/ioy115","article-title":"Thyroid hormones and female reproduction","volume":"99","author":"Silva","year":"2018","journal-title":"Biol. Reproduction"},{"key":"B25","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1016\/j.tem.2005.03.003","article-title":"Biophysical basis of pituitary cell type-specific Ca2+ signaling-secretion coupling","volume":"16","author":"Stojilkovic","year":"2005","journal-title":"Trends Endocrinol. Metab."},{"key":"B26","first-page":"165","article-title":"Status and introduction of germplasm resources for meat pigeon breeding in China","volume":"14","author":"Tang","year":"2018","journal-title":"China Livest. Poult. Breed. Industry"},{"key":"B27","doi-asserted-by":"publisher","first-page":"1181","DOI":"10.1007\/s40618-020-01230-8","article-title":"Effects of oral contraceptives on thyroid function and vice versa","volume":"43","author":"Torre","year":"2020","journal-title":"J. Endocrinol. Investigation"},{"key":"B28","doi-asserted-by":"publisher","first-page":"7069","DOI":"10.1038\/s41467-024-50809-9","article-title":"Genome-wide variation study and inter-tissue communication analysis unveil regulatory mechanisms of egg-laying performance in chickens","volume":"15","author":"Wang","year":"2024","journal-title":"Nat. Commun."},{"key":"B29","doi-asserted-by":"publisher","first-page":"R568","DOI":"10.1152\/ajpregu.00521.2006","article-title":"Hypothalamic expression of thyroid hormone-activating and -inactivating enzyme genes in relation to photorefractoriness in birds and mammals","volume":"292","author":"Watanabe","year":"2007","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1635","DOI":"10.1210\/endo-129-3-1635","article-title":"Role of the thyroid gland in seasonal reproduction. III. Thyroidectomy blocks seasonal suppression of gonadotropin-releasing hormone secretion in sheep","volume":"129","author":"Webster","year":"1991","journal-title":"Endocrinology"},{"key":"B31","doi-asserted-by":"publisher","first-page":"103317","DOI":"10.1016\/j.psj.2023.103317","article-title":"Transcriptome-based comparison reveals key genes regulating allometry growth of forelimb and hindlimb bone in duck embryos","volume":"103","author":"Wu","year":"2024","journal-title":"Poult. Sci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1159\/000066627","article-title":"Regulation of growth hormone release in common carp pituitary cells by pituitary adenylate cyclase-activating polypeptide: signal transduction involves cAMP- and calcium-dependent mechanisms","volume":"76","author":"Xiao","year":"2002","journal-title":"Neuroendocrinology"},{"key":"B33","doi-asserted-by":"publisher","first-page":"792","DOI":"10.1186\/s12864-023-09895-0","article-title":"Transcriptome analysis of hypothalamus and pituitary tissues reveals genetic mechanisms associated with high egg production rates in changshun green-shell laying hens","volume":"24","author":"Xu","year":"2023","journal-title":"BMC Genomics"},{"key":"B34","first-page":"2478","article-title":"Cloning and expression of GnIH and GnRH genes in hypothalamus of pigeons at different breeding stages","volume":"45","author":"Zhang Rui","year":"2018","journal-title":"China Animal Husb. and Veterinary Med."},{"key":"B35","doi-asserted-by":"publisher","first-page":"141","DOI":"10.3390\/genes14010141","article-title":"Interacting networks of the hypothalamic-pituitary-ovarian axis regulate layer hens performance","volume":"14","author":"Zhao","year":"2023","journal-title":"Genes (Basel)"}],"container-title":["Frontiers in Genetics"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fgene.2025.1676255\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,16]],"date-time":"2025-10-16T03:51:35Z","timestamp":1760586695000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fgene.2025.1676255\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,16]]},"references-count":35,"alternative-id":["10.3389\/fgene.2025.1676255"],"URL":"https:\/\/doi.org\/10.3389\/fgene.2025.1676255","relation":{},"ISSN":["1664-8021"],"issn-type":[{"value":"1664-8021","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,16]]},"article-number":"1676255"}}