Hypothalamic expression analysis of m6A RNA methylation associated genes suggests a potential role of epitranscriptomics in sexual maturation of Atlantic salmon

Ahi, Ehsan Pashay; Frapin, Morgane; Hukkanen, Mikaela; Primmer, Craig R.

doi:10.1016/j.aquaculture.2023.740151

Cited by 4 publications

(1 citation statement)

References 72 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…alleles associated with early (E) and late (L) maturation and the expression patterns of a number of crucial reproductive axis genes (Ahi et al 2022(Ahi et al , 2024a. 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).…”

Section: Recent Investigations In Atlantic Salmon Have Demonstrated A...mentioning

confidence: 99%

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

Pashay Ahi,

Verta,

Kurko

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

Emerging evidence suggests a link between adiposity and early maturation, potentially impacting hormonal signaling pathways governing puberty timing. Fish models have proven invaluable in studying these processes, given their genetic and physiological similarities to humans. In Atlantic salmon, in addition to being linked with environmental shifts and lipid reserves, the timing of sexual maturation also has a strong genetic basis. A gene encoding a co-factor of Hippo pathway,vgll3, is a major determinant of maturation timing in salmon, and the same gene was found to be associated with maturation timing in humans. Intriguingly,vgll3also inhibits adipogenesis in mice. Recent studies in salmon revealed correlations betweenvgll3genotypes and reproductive axis gene expression, possibly modulated through the Hippo signaling pathway. The Hippo pathway is known for its role in sexual maturation and adipogenesis and responds to environmental cues such as dietary fat and temperature. In this study, we employed a custom gene expression panel in male Atlantic salmon with differentvgll3 early(E) andlate(L) maturation genotypes testing components of this pathway in brain at immature and mature stages. We found increased brain expression of a major Hippo pathway kinase (lats1b) and melanocortin receptor encoding genes (mc4raandmc4rc) in individuals withearly(E) maturation genotypes ofvgll3before maturation development of testes. Moreover, we found components and interacting partners of Hippo pathway showing differential expression in brain of individuals withearly(E) andlate(L)vgll3genotypes prior to maturation. This could indicate extensive and complex roles of Hippo pathway in brain processes required for preparing for [the onset of] maturation at upstream of reproductive axis. This study elucidates molecular mechanisms underpinning early maturation, and for the first time in fish, offering insights into detecting it at molecular level in brain before visible gonadal changes occur.

show abstract

Section: Recent Investigations In Atlantic Salmon Have Demonstrated A...mentioning

confidence: 99%

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

Pashay Ahi,

Verta,

Kurko

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

Hippo-vgll3signaling may contribute to sex differences in Atlantic salmon maturation age via contrasting adipose dynamics

Ahi,

Verta,

Kurko

et al. 2024

Preprint

View full text Add to dashboard Cite

Sexual maturation in Atlantic salmon entails a transition in energy utilization, governed in part by genes and environmental stimuli in sex-specific manner. Salmon males require less energy, in the form of adiposity, to mature compared to females and typically mature younger. Maturation age is also influenced in a sex-dependent fashion by the vgll3 genotype (vestigial-like 3), a co-factor in the Hippo pathway. The underlying molecular processes of sex-dependent maturation age, and how they interplay with adiposity and vgll3 genotypes, have remained unknown. To elucidate the molecular mechanisms underlying sex- and genotype-specific maturation differences, we investigated the association of early (E) and late (L) maturation vgll3 alleles and the transcriptional expression of > 330 genes involved in the regulation of the Hippo pathway and sexual maturation, and related to molecular signals in brain, adipose tissue, and gonads. The strongest effect of vgll3 genotype was observed in adipose tissue for females and in brain for males, highlighting a sex-specific expression difference in the main association of vgll3 genotype. Genes related to ovarian development showed increased expression in vgll3*EE compared to vgll3*LL females. Additionally, vgll3*EE females compared to vgll3*EE males exhibited reduced markers of pre-adipocyte differentiation and lipolysis yet enhanced expression of genes related to adipocyte maturation and lipid storage. Brain gene expression further showed sex-specific expression signals for genes related to hormones and lipids, as well as tight junction assembly. Overall, these sex-specific patterns point towards a greater lipid storage and slower energy utilization in females compared to males. These results suggest that Hippo-dependent mechanisms may be important mediators of sex differences in maturation age in salmon.

show abstract

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

Ahi,

Verta,

Kurko

et al. 2024

Molecular Ecology

View full text Add to dashboard Cite

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 with different vgll3 genotypes exhibit contrasting seasonal dynamics in their lipid profiles. We also identified components of the Hippo signalling 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.

show abstract

Hypothalamic expression analysis of m6A RNA methylation associated genes suggests a potential role of epitranscriptomics in sexual maturation of Atlantic salmon

Cited by 4 publications

References 72 publications

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

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

Hippo-vgll3signaling may contribute to sex differences in Atlantic salmon maturation age via contrasting adipose dynamics

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

Contact Info

Product

Resources

About