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ARS Home » Plains Area » Clay Center, Nebraska » U.S. Meat Animal Research Center » Livestock Bio-Systems » Research » Publications at this Location » Publication #407044

Research Project: Improving Lifetime Productivity in Swine using Systems Biology and Precision Management Approaches

Location: Livestock Bio-Systems

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

Author
item WIJESENA, HIRUNI - Orise Fellow
item Keel, Brittney
item Nonneman, Danny - Dan
item Cushman, Robert - Bob
item Lents, Clay

Submitted to: Biology of Reproduction
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/19/2023
Publication Date: 10/23/2023
Citation: Wijesena, H.R., Keel, B.N., Nonneman, D.J., Cushman, R.A., Lents, C.A. 2023. Clustering of multi-tissue transcriptomes in gilts with normal cyclicity or delayed puberty reveals genes related to pubertal development. Biology of Reproduction. 110(2):261-274. Article ioad14. https://doi.org/10.1093/biolre/ioad145.
DOI: https://doi.org/10.1093/biolre/ioad145

Interpretive Summary: Sexual immaturity is a major reason for inadequate sexual behavior (estrus) in replacement gilts. Gilts that fail to display estrus are removed from the breeding herd. Understanding the physiological reasons behind sexual immaturity is important to minimize estrus failure in gilts. Scientists at Clay Center, Nebraska, compared gene expression in the tissues important for reproduction from sexually immature and mature gilts at similar ages. Researchers found critical genes in the hypothalamus, pituitary, and ovary with reduced expression in the immature gilts compared to mature gilts. This can lead to insufficient hormone production necessary for sexual development in immature gilts. These results are critical to finding better ways to optimize reproductive development of gilts and reduce the culling rate of the breeding herd.

Technical 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.