Triploidization of rainbow trout affects proteins related to ovary development and reproductive activity

Abstract

Rainbow trout are characterized by high amenability to chromosome manipulations during early development to produce androgens, gynogens, or sterile triploids, which are relevant in aquaculture. An understanding of the mechanisms affecting oogenesis and those resulting in diminished gonadal development in triploids is an important area of scientific study. Therefore, the aim of this study was to compare the ovary proteome from triploid (3 N) and diploid (2 N) rainbow trout females using tandem mass tag (TMT) peptide labelling coupled with liquid chromatography–mass spectrometry (LC–MS/MS) to identify differentially expressed proteins (DEPs) between 2 N and 3 N. The potential biological role of DEPs was also explored using comparative functional gene set enrichment to designate the potential protein markers of 3 N sterility. We identified a total of 3899 DEPs (q < 0.05), including 956 downregulated and 2943 upregulated proteins in 3 N ovaries compared to 2 N ovaries. The identified clusters for downregulated proteins in 3 N included lipid metabolic process, hormone biosynthesis, transport and exocytosis, cell junction organization and sperm-egg recognition, which can result in (i) the disruption of lipid, steroid hormone and vitellogenesis processes, (ii) impaired amino acid uptake, (iii) defects in cell–cell junctions reflecting tissue abnormalities and aberrant gonadal morphology, and (iv) impaired functions related to maintaining the proper structure of the vitelline envelope, oocyte formation and fertilization competence. With respect to upregulated proteins in 3 N ovaries, RNA processing, cell cycle, cytoskeleton organization and regulation of metabolic process were the primary clusters, which may reflect (i) the disturbance to RNA processing responsible for impairment of ovary development in triploid rainbow trout, (ii) disruption of spindle formation, incorrect chromosome alignment and segregation during meiotic division, (iii) increase in regulatory mechanism of apoptosis, which in consequence can provoke abnormal gonadal development and sterility, and (iv) enhanced ubiquitin–proteasome system governing aberrant gonadal morphology in 3 N females and oocyte maturation. The obtained results provide an accurate portrait of molecular changes in rainbow trout ovaries in response to triploidization and may contribute to a better understanding of the mechanisms responsible for impaired oogenesis in rainbow trout triploid females, which in turn leads to their sterility. Data are available via ProteomeXchange with identifier PXD034492.