Comparative transcriptome analysis identifies crucial candidate genes and pathways in the hypothalamic-pituitary-gonadal axis during external genitalia development of male geese

Abstract

Background All birds reproduce via internal fertilization, but only ~3% of male birds possess the external genitalia that allows for intromission. Waterfowl (e.g., duck and goose) are representatives of them, and the external genitalia development of male geese is directly related to mating ability. Notably, some male geese show abnormal external genitalia development during ontogenesis. However, until now little is known about the molecular mechanisms of the external genitalia development in goose. In the present study, comparative transcriptomic analyses were performed on the hypothalamus, pituitary gland, testis, and external genitalia isolated from the 245-day-old male Tianfu meat geese showing normal (NEGG, n = 3) and abnormal (AEGG, n = 3) external genitals in order to provide a better understanding of the mechanisms controlling the development of the external genitalia in aquatic bird species. Results There were 107, 284, 2192, and 1005 differentially expressed genes (DEGs) identified in the hypothalamus, pituitary gland, testis and external genitalia between NEGG and AEGG. Functional enrichment analysis indicated that the DEGs identified in the hypothalamus were mainly enriched in the ECM-receptor interaction pathway. The ECM-receptor interaction, focal adhesion, and neuroactive ligand-receptor interaction pathways were significantly enriched by the DEGs in the pituitary gland. In the testis, the DEGs were enriched in the neuroactive ligand-receptor interaction, cell cycle, oocyte meiosis, and purine metabolism. In the external genitalia, the DEGs were enriched in the metabolic, neuroactive ligand-receptor interaction, and WNT signaling pathways. Furthermore, through integrated analysis of protein-protein interaction (PPI) network and co-expression network, fifteen genes involved in the neuroactive ligand-receptor interaction and WNT signaling pathways were identified, including KNG1, LPAR2, LPAR3, NPY, PLCB1, AVPR1B, GHSR, GRM3, HTR5A, FSHB, FSHR, WNT11, WNT5A, WIF1, and WNT7B, which could play crucial roles in the development of goose external genitalia. Conclusions This study is the first systematically comparing the hypothalamus, pituitary gland, testis, and external genitalia transcriptomes of male geese exhibiting normal and abnormal external genitals. Both bioinformatic analysis and validation experiments indicated that the neuroactive ligand-receptor interaction pathway could regulate the WNT signaling pathway through PLCB1 to control male goose external genitalia development.

Gene expression of male pathway genes sox9 and amh during early sex differentiation in a reptile departs from the classical amniote model

“…One module, 7/black, strongly correlated with male development ( p -value < 0.01, correlation value > 0.7) (Figure S6 B, S9 , Table S7 ). The three most prominent hub genes, all with positive membership, were met (MET Proto-Oncogene, Receptor Tyrosine Kinase) and tiam2 (TIAM Rac1 Associated GEF 2), which have not been associated with sex differentiation, and plcb1 (Phospholipase C Beta 1) which was implicated recently in development of genitalia in male geese [ 80 ]. The next three most prominent hub genes were the transcription factor nkx3-1 and the two extracellular matrix genes fmod and col9a1 , three of the earlier mentioned genes with strong male bias in all three stages.…”

Dissociating Mechanisms That Underlie Seasonal and Developmental Programs for the Neuroendocrine Control of Physiology in Birds

“…The ECM–receptor interaction is known to play an important role in tissue and organ morphogenesis, including adipogenesis ( San et al, 2021 ). Furthermore, a recent study on the gonadal development of male geese has implicated significant enrichment of the ECM–receptor interaction pathway by differential gene expression in the pituitary gland ( Tang et al, 2022 ). Therefore, the ECM–receptor interaction pathway is a likely area for the identification of photoperiodically significant transcripts.…”

Transcriptome Analysis of the Ovaries of Taihe Black-Bone Silky Fowls at Different Egg-Laying Stages

“…LPAR3 belongs to the LPA family, which is used to encode LPA3, the third G protein-coupled receptor for lysophosphatidic acid (LPA) [ 13 ]. LPAR3 can interact with reproductive hormones to affect reproductive performance, including estrogen and progesterone [ 14 ]. Several studies have shown that LPAR3 enhances nitric oxide levels in the non-pregnant buffalo uterus and facilitates the maintenance of the corpus luteum [ 15 ].…”