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.
Highlights
Fish skeletal muscle represents up to 60% of total body mass in some species, being the most abundant tissue, responsible for their underwater propulsion and with a key role on homeostasis by acting as a protein reservoir among other functions [1, 2].Muscle growth is a multifactorial process that incorporates intrinsic and extrinsic signals in its regulation, with fibre size as a result of the balance between protein synthesis and degradation being shifted towards net protein accumulation and the activation and differentiation of myogenic progenitor cells (MPCs)
After screening all the duplicated components of the IGF-AKT-mTOR and myogenesis gene networks, we identified 20 lineage-specific ohnologs (LSOs) (11 in Ostariophysi and 9 in Acanthopterygii), with 5 related to myogenesis and 15 to the IGF-AKT-mTOR network (S1 File)
Phylogenetic analysis showed that duplicated genes were grouped in two distinctive clusters related to fish species (S2 File) following a typical topology associated to teleost whole genome duplication (TWGD) duplicated genes [50]
Summary
Fish skeletal muscle represents up to 60% of total body mass in some species, being the most abundant tissue, responsible for their underwater propulsion and with a key role on homeostasis by acting as a protein reservoir among other functions [1, 2]. In the present study we wanted to gain insights on the role that teleost WGD might have on the transcription of ohnolog genes involved on the molecular networks controlling muscle growth, and try to estimate the impact of neofunctionalization, subfunctionalization and redundancy on their regulation. To achieve these objectives and to correctly interpret the results obtained we used LSOs differently retained between Ostariophysi and Acanthopterygii superorders. Juveniles from both species were used on a fasting-refeeding experiment to manipulate growth rate [57,58,59]
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