An insight on the impact of teleost whole genome duplication on the regulation of the molecular networks controlling skeletal muscle growth

Abstract

Fish muscle growth is a complex process regulated by multiple pathways, resulting on the net accumulation of proteins and the activation of myogenic progenitor cells. Around 350–320 million years ago, teleost fish went through a specific whole genome duplication (WGD) that expanded the existent gene repertoire. Duplicated genes can be retained by different molecular mechanisms such as subfunctionalization, neofunctionalization or redundancy, each one with different functional implications. While the great majority of ohnolog genes have been identified in the teleost genomes, the effect of gene duplication in the fish physiology is still not well characterized. In the present study we studied the effect of WGD on the transcription of the duplicated components controlling muscle growth. We compared the expression of lineage-specific ohnologs related to myogenesis and protein balance in the fast-skeletal muscle of pacus (Piaractus mesopotamicus—Ostariophysi) and Nile tilapias (Oreochromis niloticus—Acanthopterygii) fasted for 4 days and refed for 3 days. We studied the expression of 20 ohnologs and found that in the great majority of cases, duplicated genes had similar expression profiles in response to fasting and refeeding, indicating that their functions during growth have been conserved during the period after the WGD. Our results suggest that redundancy might play a more important role in the retention of ohnologs of regulatory pathways than initially thought. Also, comparison to non-duplicated orthologs showed that it might not be uncommon for the duplicated genes to gain or loss new regulatory elements simultaneously. Overall, several of duplicated ohnologs have similar transcription profiles in response to pro-growth signals suggesting that evolution tends to conserve ohnolog regulation during muscle development and that in the majority of ohnologs related to muscle growth their functions might be very similar.

Identification of Novel Genes Associated with Fish Skeletal Muscle Adaptation during Fasting and Refeeding Based on a Meta-Analysis

“…The experiments were carried out on animals and their muscle tissue from previous studies [ 6 , 16 ] according to the ARRIVE [ 29 ] guidelines and those of the Brazilian National Council for the Control of Animal Experimentation (CONCEA). The protocol was approved by the Ethics Committee on Animal Use (protocol numbers 705 and 1050) of the Institute of Biosciences, São Paulo State University (UNESP), Botucatu, São Paulo, Brazil.…”

“…The fish were reared at 28 °C under a natural photoperiod (12 h light:12 h dark) in different recirculation systems in 0.5 m 3 tanks containing 30 pacus. All the fish underwent a 15-day adaptation period with ad libitum food two to three times a day, following the diet previously described in the publications of our research group [ 6 , 16 ], before the start of the experiments.…”

“…In this context, the lengths of the fasting and refeeding periods were selected based on the size of the fish, considering that these nutritional changes would modify the muscle transcriptional signature without triggering the death of the fish before their experimental evaluation. In addition to these aspects, our research group has already obtained significant results by evaluating the classical genes of the skeletal muscle in these periods of fasting and refeeding in pacus [ 6 , 16 ], suggesting that evaluations of novel genes in these experimental models can be of great value for the area. After the experiments, the pacus were euthanized with excess benzocaine (Sigma Aldrich, St. Louis, MO, USA) at a concentration up to and exceeding 250 mg/L, and the fast-twitch muscles were collected from each experimental group (5 fish/experimental group).…”

“…In addition, improvements in management techniques developed through studies seeking to understand how aspects of the cultivation environment affect the development of this species have contributed to the high level of pacu production [ 4 ]. Recently published in vivo and in vitro studies explored the genetic attributes that regulate the fast growth and impressive musculature of this species [ 5 , 6 ], with the pacu presenting an excellent model for studies of the skeletal muscle [ 7 ].…”

Teleostean fishes may have developed an efficient Na+ uptake for adaptation to the freshwater system

“…However, ENaC genes and ENaC-mediated Na + uptake function are not found in teleosts ( Figure 1 ) ( Hwang and Perry, 2010 ; Hwang et al, 2011 ). Although there have been major advances in understanding how the evolutionary success of teleosts with the additional teleosts-specific whole-genome duplication (TWGD) ( Jaillon et al, 2004 ), the direct involvement of TWGD in every variety of teleosts physiological significances by the enrolled epithelial channels/transporters has so far been overlooked ( Lin et al, 2020 ; Duran et al, 2021 ). Since the Na + regulation is an essential physiological event and fundamental driving force requisite of any transepithelial transport, homeostasis is impossible without it.…”