Gene co-expression patterns in Atlantic salmon adipose tissue provide a molecular link among seasonal changes, energy balance and age at maturity

Abstract

Sexual maturation in many fishes requires a major physiological change that involves a rapid transition between energy storage and usage. In Atlantic salmon, this transition for the initiation of maturation is tightly controlled by seasonality and requires a high-energy status . Lipid metabolism is at the heart of this transition since lipids are the main energy storing molecules. The balance between lipogenesis (lipid accumulation) and lipolysis (lipid use) determines energy status transitions. A genomic region containing a transcription co-factor of the Hippo pathway, vgll3, is the main determinant of maturation timing in Atlantic salmon. Interestingly, vgll3 acts as an inhibitor of adipogenesis in mice and its genotypes are potentially associated with seasonal heterochrony in lipid storage and usage in juvenile Atlantic salmon. Here, we explored changes in expression of more than 300 genes directly involved in the processes of adipogenesis, lipogenesis and lipolysis, as well as the Hippo pathway in the adipose tissue of immature and mature Atlantic salmon with distinct vgll3 genotypes. We found molecular evidence consistent with a scenario in which immature males exhibiting vgll3 genotype specific seasonal direction of change in their lipid profiles. We also identified components of the Hippo signaling pathway as potential major drivers of vgll3 genotype specific differences in adipose tissue gene expression. This study demonstrates the importance of adipose gene expression patterns for directly linking environmental changes with energy balance and age at maturity through genetic factors bridging lipid metabolism, seasonality and sexual maturation.

A salmon fish model reveals genetic signals in brain associated with early maturation

“…The anticipation that vgll3 genotype effects on reproductive axis genes may be modulated through divergent Hippo signaling pathway activation has been shown by gene co-expression network analysis (Ahi et al 2023). The Hippo pathway is rapidly emerging not only as a pivotal molecular signal governing sexual maturation in vertebrates (Kjaerner-Semb et al 2018;Sen Sharma et al 2019;Kurko et al 2020) but also as a regulator in the equilibrium between adipocyte proliferation and differentiation (Ahi et al 2024b). Moreover, the Hippo pathway seems to play an integral role in transducing environmental cues, such as alterations in dietary fat content and temperature, into transcriptional responses (Shu et al 2019;Luo et al 2020).…”

“…In addition to its role in maturation age, vgll3 serves as an inhibitor of adipogenesis in mice (Halperin et al 2013). In salmon, individuals with distinct vgll3 genotypes exhibit seasonal variations in energy storage, suggesting a noteworthy link between energy utilization and environmental changes (House et al 2023;Ahi et al 2024b).…”