Salmonid genomes have a remarkably expandedakirinfamily, coexpressed with genes from conserved pathways governing skeletal muscle growth and catabolism

Abstract

Metazoan akirin genes regulate innate immunity, myogenesis, and carcinogenesis. Invertebrates typically have one family member, while most tetrapod and teleost vertebrates have one to three. We demonstrate an expanded repertoire of eight family members in genomes of four salmonid fishes, owing to paralog preservation after three tetraploidization events. Retention of paralogs secondarily lost in other teleosts may be related to functional diversification and posttranslational regulation. We hypothesized that salmonid akirins would be transcriptionally regulated in fast-twitch skeletal muscle during activation of conserved pathways governing catabolism and growth. The in vivo nutritional state of Arctic charr (Salvelinus alpinus L.) was experimentally manipulated, and transcript levels for akirin family members and 26 other genes were measured by quantitative real-time PCR (qPCR), allowing the establishment of a similarity network of expression profiles. In fasted muscle, a class of akirins was upregulated, with one family member showing high coexpression with catabolic genes coding the NF-kappaB p65 subunit, E2 ubiquitin-conjugating enzymes, E3 ubiquitin ligases, and IGF-I receptors. Another class of akirin was upregulated with subsequent feeding, coexpressed with 14-3-3 protein genes. There was no similarity between expression profiles of akirins with IGF hormones or binding protein genes. The level of phylogenetic relatedness of akirin family members was not a strong predictor of transcriptional responses to nutritional state, or differences in transcript abundance levels, indicating a complex pattern of regulatory evolution. The salmonid akirins epitomize the complexity linking the genome to physiological phenotypes of vertebrates with a history of tetraploidization.

Growth and the regulation of myotomal muscle mass in teleost fish

“…The role of the IGF-Akt pathway in inhibiting atrophy appears conserved in teleosts, as IGF-I induced phosphorylation of both Akt and FOXO proteins and concurrent downregulation of MuRF1 and MAFbx was observed in salmonids (Cleveland and Weber, 2010;Seiliez et al, 2010). The NF-kB pathway may also have a role in controlling protein breakdown in salmonids, as there was a large increase in mRNA expression of both p65 (a subunit of the NF-kB complex) and the NF-kB target genes MuRF1 and UBE2H during fasting (Macqueen et al, 2010a;Bower and Johnston, 2010b). Our understanding of both these pathways in teleosts is in its infancy and both warrant considerable further attention.…”

“…In salmonids, a family of eight paralogues is present (compared with two in mammals) as a result of the two WGD events (Macqueen et al, 2010a). In both the fast muscle of adult Arctic charr (Macqueen et al, 2010a) and a primary myogenic cell culture derived from adult Atlantic salmon fast muscle (Macqueen et al, 2010b), akirin paralogues originating from the salmonid WGD event (the most recent paralogues), were typically less coregulated than were more distant paralogues (e.g. paralogues separated from WGD events at the base of teleosts or even vertebrates).…”

Evolution of akirin family in gene and genome levels and coexpressed patterns among family members and rel gene in croaker

“…To date, akirin genes are identified from eukaryotes, including coelenterates, arthropods, fish, amphibians, birds, reptiles, and mammals (Chen et al, 2012;Dai et al, 2011;Goto et al, 2008;Macqueen et al, 2010aMacqueen et al, , 2010bMan et al, 2011;Yang et al, 2011). Furthermore, the akirin gene family consists of two members in amphibians and mammals (akirin1 and akirin2), a single member in birds and reptiles (akirin2), and two to three members in teleosts (akirin1(1) and akirin2(1) and/ or akirin2(2)) (Macqueen et al, 2010a(Macqueen et al, , 2010b. However, teleost species of the Salmonidae family include eight akirin family members (akirin1(1a), 1(1b), 1(2a), 1(2b), 2(1a), 2(1b), 2(2a), and 2(2b)) (Macqueen et al, 2010a).…”

“…Furthermore, the akirin gene family consists of two members in amphibians and mammals (akirin1 and akirin2), a single member in birds and reptiles (akirin2), and two to three members in teleosts (akirin1(1) and akirin2(1) and/ or akirin2(2)) (Macqueen et al, 2010a(Macqueen et al, , 2010b. However, teleost species of the Salmonidae family include eight akirin family members (akirin1(1a), 1(1b), 1(2a), 1(2b), 2(1a), 2(1b), 2(2a), and 2(2b)) (Macqueen et al, 2010a). Meanwhile, Macqueen and Johnston (2009) and Macqueen et al (2010a) proposed that the number of akirin gene family members is closely related with whole genome duplications (WGDs).…”

“…However, teleost species of the Salmonidae family include eight akirin family members (akirin1(1a), 1(1b), 1(2a), 1(2b), 2(1a), 2(1b), 2(2a), and 2(2b)) (Macqueen et al, 2010a). Meanwhile, Macqueen and Johnston (2009) and Macqueen et al (2010a) proposed that the number of akirin gene family members is closely related with whole genome duplications (WGDs). Akirin1 and akirin2 are derived from basal vertebrate WGD (2R) (Putnam et al, 2008).…”