Clustering of multi-tissue transcriptomes in gilts with normal cyclicity or delayed puberty reveals genes related to pubertal development

Abstract In gilts, puberty is marked by standing estrus in the presence of a boar. Delayed puberty (DP; failure to display pubertal estrus) is a major reason for gilt removal. To investigate the physiological determinants underlying DP in gilts, transcriptomic data from tissues relevant to estrus an...

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Bibliographic Details
Published in:Biology of reproduction 2024-02, Vol.110 (2), p.261-274
Main Authors: Wijesena, Hiruni R, Keel, Brittney N, Nonneman, Dan J, Cushman, Robert A, Lents, Clay A
Format: Article
Language:English
Subjects:
Amygdala
Animals
Cbfa-1 protein
Cortex (olfactory)
Estrus cycle
Female
Folliculogenesis
Gene expression
Gonadotropins
Hypothalamus (anterior)
Hypothalamus - metabolism
Luteinizing hormone
Luteinizing Hormone - metabolism
Male
Olfactory bulb
Ovaries
Pituitary (anterior)
Puberty
Sexual Maturation - genetics
Steroidogenesis
Sus scrofa - metabolism
Swine
Transcriptome
Transcriptomes
Transcriptomics
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Summary:Abstract In gilts, puberty is marked by standing estrus in the presence of a boar. Delayed puberty (DP; failure to display pubertal estrus) is a major reason for gilt removal. To investigate the physiological determinants underlying DP in gilts, transcriptomic data from tissues relevant to estrus and puberty, such as mediobasal hypothalamus, anterior pituitary gland, ovarian cortex, olfactory bulb, amygdala, and hippocampus, were obtained from age-matched DP (n = 8) and cyclic control gilts at follicular phase (n = 8) and luteal phase (n = 8) of the estrous cycle. A gene expression module analysis via three-way gene × individual × tissue clustering using tensor decomposition identified pituitary and ovary gene modules contributing to regulation of pubertal development. Analysis of gene expression in the hypothalamic–pituitary–ovary axis identified reduced expression of hypothalamic genes critical for stimulating gonadotropin secretion (KISS1 and TAC3) and reduced expression of LHB in the anterior pituitary of DP gilts compared with their cyclic counterparts. Consequently, luteinizing hormone-induced genes in the ovary important for folliculogenesis (OXTR, RUNX2, and PTX3) were less expressed in DP gilts. Other intrafollicular genes (AHR, PTGS2, PTGFR, and IGFBP7) and genes in the steroidogenesis pathways (STAR and CYP11A1) necessary to complete the ovulatory cascade were also less expressed in DP gilts. This is the first clustering of multi-tissue expression data from DP and cyclic gilts to identify genes differentially expressed in gilts of similar ages but at different levels of sexual development. A critical lack of gonadotropin support and reduced ovarian responsiveness underlie DP in gilts. Clustering of multi-tissue expression data and differential gene expression analysis of delayed puberty and normal cyclic gilts identified genes in the hypothalamic–pituitary–ovary axis associated with sexual maturity, development, and estrous cycle functions. Graphical Abstract Graphical Abstract
ISSN:0006-3363
1529-7268
DOI:10.1093/biolre/ioad145