Abstract
The pituitary is a remarkably dynamic organ with roles in hormone (FSH and LH) synthesis and secretion. In animals with the FecB (fecundity Booroola) mutation, the pituitary experiences hormone fluctuations during the follicular–luteal transition, which is implicated in the expression and regulation of many genes and regulators. Long non-coding RNAs (lncRNAs) are a novel type of regulatory factors for the reproductive process. Nevertheless, the expression patterns of lncRNAs and their roles in FecB-mediated follicular development and ovulation remain obscure. Thus, we profiled the pituitary transcriptome during the follicular (F, 45 h after evacuation vaginal sponges) and luteal (L, 216 h after evacuation vaginal sponges) phases in FecB-mutant homozygous (BB) and wild-type (WW) Small Tail Han sheep. We identified 78 differentially expressed genes (DEGs) and 41 differentially expressed lncRNAs (DELs) between BB_F and BB_L, 32 DEGs and 26 DELs between BB_F and WW_F, 16 DEGs and 29 DELs between BB_L and WW_L, and 50 DEGs and 18 DELs between WW_F and WW_L. The results of real-time quantitative PCR (RT-qPCR) correlated well with the transcriptome data. In both the follicular and luteal phases, DEGs (GRID2, glutamate ionotropic receptor delta type subunit 2; ST14, ST14 transmembrane serine protease matriptase) were enriched in hormone synthesis, secretion, and action. MSTRG.47470 and MSTRG.101530 were the trans-regulated elements of ID1 (inhibitor of DNA binding 3, HLH protein) and the DEG ID3 (inhibitor of DNA binding 3, HLH protein), and EEF2 (eukaryotic translation elongation factor 2), respectively; these factors might be involved in melatonin and peptide hormone secretion. In the FecB-mediated follicular phase, MSTRG.125392 targeted seizure-related 6 homolog like (SEZ6L), and MSTRG.125394 and MSTRG.83276 targeted the DEG KCNQ3 (potassium voltage-gated channel subfamily Q member 3) in cis, while MSTRG.55861 targeted FKBP4 (FKBP prolyl isomerase 4) in trans. In the FecB-mediated luteal phase, LOC105613905, MSTRG.81536, and MSTRG.150434 modulated TGFB1, SMAD3, OXT, respectively, in trans. We postulated that the FecB mutation in pituitary tissue elevated the expression of certain genes associated with pituitary development and hormone secretion. Furthermore, this study provides new insights into how the pituitary regulates follicular development and ovulation, illustrated by the effect of the FecB mutation.
Highlights
The FecB mutation was first detected in high-fecundity Australian Booroola Merino sheep [1]
The raw RNA sequencing (RNA-seq) data from the Small Tail Han sheep were analyzed for quality control before aligning reads to the reference genome
We identified the essential features of the long non-coding RNAs (lncRNAs) and contrasted them with those of messenger RNA (mRNA)
Summary
The FecB (fecundity Booroola) mutation was first detected in high-fecundity Australian Booroola Merino sheep [1]. Through an impairment of the activity of the BMPR1B receptor kinase, FecB mutation weakened the inhibitory effect of the BMPR1B gene on steroid synthesis in granulosa cells, leading to the maturation and ovulation of ovulatory follicles at significantly small diameters and fewer granulosa cells in homozygous FecB sheep than those in non-FecB sheep [2, 3, 5,6,7]. A previous study predicted that FecB might impact the pituitary gland through the regulation of hormone release during one estrus cycle in ewes [10]. The identification of the key regulators of these developmental processes could be beneficial for understanding the mechanisms of how FecB regulates the follicular–luteal transition at the molecular level and for screening candidate protein-coding genes with impacts on reproductive ability in ewes
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