Effects of feeding level and sexual maturation on expression of genes regulating growth mechanisms in rainbow trout (Oncorhynchus mykiss)

Authors: Weber, Gregory - Greg; Ma, Hao; Birkett, Jill; Cleveland, Beth

Submitted to: Aquaculture
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/9/2022
Publication Date: 1/13/2022
Citation: Weber, G.M., Ma, H., Birkett, J.E., Cleveland, B.M. 2022. Effects of feeding level and sexual maturation on expression of genes regulating growth mechanisms in rainbow trout (Oncorhynchus mykiss). Aquaculture. 551: 737917. https://doi.org/10.1016/j.aquaculture.2022.737917.
DOI: https://doi.org/10.1016/j.aquaculture.2022.737917

Interpretive Summary: The eggs of a fully mature female rainbow trout can weigh as much as 20% of its entire body weight. Therefore, the energy and nutrient demands of sexual maturation in salmonids such as rainbow trout requires a shift from somatic growth to gonadal development that can result in a dramatic loss in body weight as body fat and muscle mass is mobilized to provide energy and nutrients for egg growth. Severe loss of nutrients including fat and protein from muscle can result in reduced fillet quality and also negatively impact the ability of the fish to recover after spawning. Although a loss in skeletal muscle can be avoided with adequate nutrition, how nutrient availability or ration affects the endocrine and growth factor systems that integrate nutrient partitioning, muscle metabolism, and growth during sexual maturation is poorly understood. The primary objective of this study was to determine how ration affects gene expression of the endocrine systems that regulate sexual maturation, growth, and metabolism, in order to better understand physiological mechanisms associated with nutrient and energy partitioning during gonadal development. These genes include estradiol receptors (ERs), components of the GH/IGF axis and the TGFbeta superfamily system, and muscle specific regulatory factors. In summary, moderate feeding appears to counter many changes in endocrine and growth factor system gene expression associated with growth reduction during maturation, perhaps altering endocrine and growth factor regulation to spare peripheral tissues from wasting and better preparing the fish for post-spawning recovery.

Technical Abstract: The energy and nutrient demands of sexual maturation in salmonids requires a shift from somatic growth to gonadal development, although a loss in skeletal muscle can be avoided with adequate nutrition. How nutrient availability or ration affects the endocrine and growth factor systems that integrate nutrient partitioning, muscle metabolism, and growth during sexual maturation is poorly understood. In the current study female diploid rainbow trout (Oncorhynchus mykiss) approaching ovulation were fed for 12 weeks at 0.25% and 0.50% tank biomass, and to apparent satiation. Controls for the effects of gonadal development included sterile triploid trout that were fed at the 0.50% level, and two diploid females fed at the 0.25% level that failed to undergo gonadal development. Primary objectives were to determine how sexual maturation and ration affect expression of estradiol (E2) receptors (ERs), components of the growth hormone/insulin-like growth factor (GH/IGF) axis and the transforming growth factor-beta (TGFbeta) superfamily system, and muscle specific regulatory factors to better understand physiological mechanisms associated with nutrient and energy partitioning during gonadal development. Expression of era1 was highly increased in muscle of maturing diploids suggesting an increase in the catabolic effects of E2 on muscle. In the liver, expression of era2 had the greatest increase with maturation, but expression of all ERs were increased with higher rations suggesting improved E2 sensitivity for vitellogenin production. Hepatic expression of ghrs and igfs were generally reduced with maturation suggesting a reduction in systemic growth promotion. Increased ration improved capacity for IGF signaling in muscle via increased igf1 and igfr1b expression, potentially lessening effects of reduced circulating IGF-I on muscle growth. The primary carrier of IGFs, hepatic igfbp2b1, increased with maturation likely reducing systemic IGF activity, and was also elevated with higher rations. All other hepatic IGFBPs except igfbp1 showed some reduction with maturation and several increased with increased ration. Increased muscle igfbp6b1 suggests restricted myogenesis with maturation. Reductions in expression of muscle specific regulators with maturation including pax7a, myog and myf5, support reduced myogenesis with maturation but were unaffected by ration. In addition, although mstn2a was the only myostatin (MSTN) gene affected by maturation or ration, altered expression of components of the TGFbeta superfamily suggest increased ration may inhibit MSTN signaling. In summary, moderate feeding appears to counter many changes in endocrine and growth factor system gene expression associated with growth reduction during maturation, perhaps altering endocrine and growth factor regulation to spare peripheral tissues from wasting and better preparing the fish for post-spawning recovery.