Resolving the complexity of vitellogenins and their receptors in the tetraploid Atlantic salmon (Salmo salar): Ancient origin of the phosvitin‐less VtgC in chondrichthyean fishes

Abstract

Egg yolk proteins are mainly derived from vitellogenin (Vtg), and serve as essential nutrients during early development in oviparous organisms. Vertebrate Vtgs are predominantly synthesized in the liver of maturing females, and are internalized by the oocyte after binding to specific surface receptors (VtgR). Here, we clarify the evolutionary history of vertebrate Vtgs, including the teleost VtgC, which lacks phosvitin, and investigate the repertoire of Vtgs and VtgRs in the tetraploid Atlantic salmon (Salmo salar). Conserved synteny of the vtg genes in elephant fish (Callorhinchus milii) strongly indicates that the vtg gene cluster was present in the ancestor of tetrapods and ray-finned fish. The shortened phosvitin in the VtgC ortholog of this chondrichthyean fish may have resulted from early truncation events that eventually allowed the total disappearance of phosvitin in teleost VtgC. In contrast, the tandem-duplicated VtgCs identified in the spotted gar (Lepisosteus oculatus) both contain the phosvitin domain. The Atlantic salmon genome harbors four vtg genes encoding the complete VtgAsa1, phosvitin-less VtgC, and truncated VtgAsb proteins; vtgAsa2 is a pseudogene. The three vtg genes were mainly expressed in the liver of maturing females, and the vtgAsa1 transcript predominated prior to spawning. The splice variant lacking the O-linked sugar domain dominated ovarian expression of vtgr1 and vtgr2. Strongly increased vtgAsa1 expression during vitellogenesis contrasted with the peaks of vtgr1 and vtgr2 in the previtellogenic oocytes, which gradually decreased over the same period. Recycling of the oocyte VtgRs is probably not sufficient to maintain receptor number during vitellogenesis.

Ultrasound as a noninvasive tool for monitoring reproductive physiology in female Atlantic salmon (Salmo salar )

“…Recently, high expression of vitellogenin receptors in ovaries from females during the same period have been observed, supporting our observation (Andersen et al. ) The early development of vitellogenic oocytes found here appears to be more similar to observations in rainbow trout ( Oncorhynchus mykiss ; Sumpter et al. ).…”

“…This is somewhat earlier than expected compared to other studies in Atlantic salmon females, where secondary growth phase oocytes were observed equally early under similar photoperiod treatment, but not any vitellogenic oocytes (Taranger et al 1998(Taranger et al , 1999Andersson et al 2009). Recently, high expression of vitellogenin receptors in ovaries from females during the same period have been observed, supporting our observation (Andersen et al 2017) The early development of vitellogenic oocytes found here appears to be more similar to observations in rainbow trout (Oncorhynchus mykiss; Sumpter et al 1984).…”

Genome editing reveals reproductive and developmental dependencies on specific types of vitellogenin in zebrafish (Danio rerio)

“…Jawed vertebrates produce three major forms of Vtg arising from a vtg gene cluster that was present in the ancestor of tetrapods and ray-finned fish (Babin, 2008; Finn et al, 2009). During vertebrate evolution these ancestral vtg genes were subject to whole genome duplications, loss of paralogs and lineage-specific tandem duplications, giving rise to substantial variation in the repertoire and number of vtg genes present in an individual species, especially among teleost fish (Andersen et al, 2017). The linear yolk protein domain structure of complete teleost Vtgs is: NH 2 -lipovitellin heavy chain (LvH)-phosvitin (Pv)-lipovitellin light chain (LvL)-beta component (β’c)-C-terminal component (Ct)-COOH (Patiño and Sullivan, 2002; Hiramatsu et al, 2005).…”

Genome editing reveals reproductive and developmental dependencies on specific types of vitellogenin in zebrafish (Danio rerio)

“…Jawed vertebrates produce three major forms of Vtg arising from a vtg gene cluster that was present in the ancestor of tetrapods and ray-finned fish (Babin, 2008;Finn, Kolarevic, Kongshaug, & Nilsen, 2009). During vertebrate evolution these ancestral vtg genes were subject to whole genome duplications, loss of paralogs and lineage-specific tandem duplications, giving rise to substantial variation in the repertoire and number of vtg genes present in an individual species, especially among teleost fish (Andersen et al, 2017). The linear yolk protein domain structure of complete teleost Vtgs is NH 2 -lipovitellin heavy chain (LvH)phosvitin (Pv)-lipovitellin light chain (LvL)-β component (β'c)-C-terminal component (Ct)-COOH (Hiramatsu, Cheek, Sullivan, Matsubara, & Hara, 2005;Patiño & Sullivan, 2002).…”