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Strong regulatory effects of vgll3 genotype on reproductive axis gene expression in juvenile male Atlantic salmon
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Animal experimentation followed European Union Directive 2010/63/EU under license ESAVI/42575/2019 granted by the Animal Experiment Board in Finland (ELLA).. International audience. Highlights: • Age at maturity contributes to the diversity of life history strategies and the maturation process influences the production of sex hormones and behavior. • Alternative alleles of the vgll3 gene associate with maturation timing in Atlantic salmon. • We show that there is strong vgll3 genotype-dependent differential expression of reproductive axis genes, including gonadotropins. • The effects of vgll3 alleles on the transcription of genes controlling spermatogenesis are not sufficient for initiating testis maturation.Abstract: Age at maturity is a major contributor to the diversity of life history strategies in organisms. The process of maturation is influenced by both genetics and the environment, and includes changes in levels of sex hormones and behavior, but the specific factors leading to variation in maturation timing are poorly understood. gnrh1 regulates the transcription of gonadotropin genes at pubertal onset in many species, but this gene is lacking in certain teleost species including Atlantic salmon (Salmo salar), which raises the possibility of the involvement of other important regulatory factors during this process. Earlier research has reported a strong association of alternative alleles of the vgll3 gene with maturation timing in Atlantic salmon, suggesting it as a potential candidate regulating reproductive axis genes. Here, we investigated the expression of reproductive axis genes in one-year-old Atlantic salmon males with immature gonads and different vgll3 genotypes during the spawning period. We detected strong vgll3 genotype-dependent differential expression of reproductive axis genes (such as fshb, lhb, amh and igf3) tested in the pituitary, and testis. In addition, we observed differential expression of jun (ap1) and nr5a1b (sf1), potential upstream regulators of gonadotropins in the pituitary, as well as axin2, id3, insl3, itch, ptgs2a and ptger4b, the downstream targets of amh and igf3 in the testis. Hereby, we provide evidence of strong vgll3 genotype-dependent transcriptional regulation of reproductive axis genes prior to sexual maturation and suggest alternative models for distinct actions of vgll3 genotypes on the related molecular processes.
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