Abstract
In all vertebrates studied so far, germ cells are not required for pubertal maturation of the gonadal steroidogenic system, subsequent development of secondary sex characteristics and reproductive behavior. To explore if the absence of germ cells affects puberty or growth in Atlantic salmon, germ cell-free (GCF), dnd knockout and wild type (WT) postsmolts were stimulated to enter puberty. No GCF fish entered puberty, whereas 66.7% (males) and 30% (females) WT fish completed or entered puberty, respectively. Expression of genes related to steroidogenesis (star, cyp17a1, cyp11β, cyp19a1a), gonadal somatic cells (insl3, amh, igf3), oocytes (bmp15), gonadotropin receptors (fshr, lhcgr), and pituitary gonadotropic cells (fshb, lhb, gnrhr4) showed an immature status and failure to up-regulate gonadal sex steroid production in male and female GCF fish was also reflected in low or undetectable plasma sex steroids (11-ketotestosterone, estradiol-17β and testosterone). A gender difference (high in females, low in males) was found in the expression of star and cyp17a1 in GCF fish. No clear difference in growth was detected between GCF and immature WT fish, while growth was compromised in maturing WT males. We demonstrate for the first time in a vertebrate that germ cells are required for pubertal activation of the somatic steroidogenic cells.
Highlights
Teleost fish share many homologies with other vertebrates, including the basic building blocks of the endocrine system regulating reproductive processes via the brain-pituitary-gonad (BPG) axis[1,2,3]
While it is known that Sertoli cells – a somatic cell type in the testis - express growth hormone (Gh) in both tilapia and Japanese eel, studies in tilapia have shown that growth hormone receptors are expressed by germ cells[8,9], and might respond to Gh by producing Igf family members[10]
We have explored the phenotype of dnd knockout and germ cell-free (GCF), sterile male salmon[11], exposed to an established postsmolt maturation regime, usually inducing sexual maturation in 50–90% of the males in different families of Atlantic salmon[17,18,19]
Summary
Complete loss of germ cells in all vertebrates studied so far resulted in sterility, while other gonadal functions, such as sex steroid production, remain intact[4], followed by development of secondary sex characteristics[5,6,7]. The initiation of puberty in females is accompanied by an increase in pituitary fshb, plasma E2 and a transition from the “oildrop” immature stage to the beginning of vitellogenesis, characterized by primary yolk vesicles in the ovary[23] Histological analysis revealed both immature (Fig. 3a; 70%) and early vitellogenic (Fig. 3b; 30%) females in the WT fish exposed to the maturation regime. A similar pattern was observed regarding the GSI, which was low in GCF females, higher in the immature WT group and highest in the early vitellogenic WT fish (Fig. 1c) This shows that a significant proportion of the WT females were entering puberty in response to the maturation regime, while none of the GCF females showed any signs of puberty. The igf[3] transcript levels were
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