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Genes Encoding Teleost Fish Ligands and Associated Receptors Remained in Duplicate More Frequently than the Rest of the Genome.

ABSTRACT: Signaling through ligand/receptor interactions is a widespread mechanism across all living taxa. During evolution, however, there has been a diversification in multigene families and changes in their interaction patterns. Among the events that led to the creation of new genes is the whole-genome duplication, which made possible some major innovations. Teleost fishes descended from a common ancestor which underwent one such whole-genome duplication. In our study, we investigated the effect of complete genome duplication on the evolution of ligand-receptor pairs in teleosts. We selected ten teleost species and used bioinformatics programs and phylogenetic tools in order to study the evolution of the human ligands and receptors that have orthologous genes in fishes, as well as the rest of the fish genomes. We established that since the complete duplication of the fish genomes, the conservation in duplicate copy of ligand and receptor genes is higher than expected. However, the ligand/receptor pair partners did not necessarily evolve in the same way, and a lot of situations occurred in which one of the partners returned in singleton copy when the other one was maintained in duplicate. This suggests that changes in interaction partners may have taken place during the evolution of teleosts. Moreover, the fate of the ligands and receptor coding genes is partly congruent with the phylogeny of teleosts. However, some incongruences can be observed. We suggest that these incongruences are correlated to the environment.

SUBMITTER: Grandchamp A

PROVIDER: S-EPMC6540934 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Cell signalling involves a myriad of proteins, many of which belong to families of related proteins, and these proteins display a huge number of interactions. One of the events that has led to the creation of new genes is whole genome duplication (WGD), a phenomenon that has made some major innovations possible. In addition to the two WGDs that happened before gnathostome radiation, teleost genomes underwent one (the 3WGD group) or two (the 4WGD group) extra WGD after separation from the lineage leading to holostei. In the present work, we studied in 63 teleost species whether the orthologues of human genes involved in 47 signalling pathways (HGSP) remain more frequently duplicated, triplicated or in the singleton state compared with the whole genome. We found that these genes have remained duplicated and triplicated more frequently in teleost of the 3WGD and 4WGD groups, respectively. Moreover, by examining pairs of interacting gene products in terms of conserved copy numbers, we found a majority of the 1:1 and 1:2 proportions in the 3WGD group (between 54% and 60%) and of the 2:2 and 2:4 proportions in the 4WGD group (30%). In both groups, we observed the 0:n proportion at a mean of approximately 10%, and we found some pseudogenes in the concerned genomes. Finally, the proportions were very different between the studied pathways. The n:n (i.e. same) proportion concerned 20%-65% of the interactions, depending on the pathways, and the n:m (i.e. different) proportion concerned 34%-70% of the interactions. Among the n:n proportion, the 1:1 ratio is most represented (25.8%) and among the n:m ratios, the 1:2 is most represented (25.0%). We noted the absence of gene loss for the JAK-STAT, FoxO and glucagon pathways. Overall, these results show that the teleost gene orthologues of HGSP remain duplicated (3WGD) and triplicated (4WGD) more frequently than the whole genome, although some genes have been lost, and the proportions have not always been maintained.

Project description:Interleukin-17 (IL-17) cytokine comprises a family of six ligands in mammals with proinflammatory functions, having an important role in autoimmune disorders and against bacterial, viral, and fungal pathogens. While IL-17A and IL-17F ligands are mainly produced by Th cells (Th17 cells), the rest of the ligands are expressed by other immune and non-immune cells and have different functions. The identification of IL-17 ligands in fish has revealed the presence of six members, counterparts to mammalian ones, and a teleost-specific form, the fish IL-17N. However, tissue distribution, the regulation of gene expression, and scarce bioactivity assays point to similar functions compared to mammalian ones, though this yet to be investigated and confirmed. Thus, we have identified seven IL-17 ligands in the teleost European sea bass (Dicentrarchus labrax), for the first time, corresponding to IL-17A/F1, IL-17A/F2, IL-17A/F3, IL-17C1, IL-17C2, IL-17D, and IL-17N, according to the predicted protein sequences and phylogenetic analysis. They are constitutively and widely transcribed in sea bass tissues, with some of them being mainly expressed in the thymus, brain or intestine. Upon in vitro stimulation of head-kidney leucocytes, the mRNA levels of all sea bass IL-17 ligands were up-regulated by phytohemagglutinin treatment, a well-known T cell mitogen, suggesting a major expression in T lymphocytes. By contrast, the infection of sea bass juveniles with nodavirus (NNV), a very pathogenic virus for this fish species, resulted in the up-regulation of the transcription of IL-17C1 in the head-kidney and of IL-17C1 and IL-17D in the brain, the target tissue for NNV replication. By contrast, NNV infection led to a down-regulated transcription of IL-17A/F1, IL-17A/F2, IL-17C1, IL-17C2, and IL-17D in the head-kidney and of IL-17A/F1 and IL-17A/F3 in the brain. The data are discussed accordingly with the IL-17 ligand expression and the immune response under the different situations tested.

Project description:BackgroundDuplication and subsequent neofunctionalization of the teleostean hatching enzyme gene occurred in the common ancestor of Euteleostei and Otocephala, producing two genes belonging to different phylogenetic clades (clade I and II). In euteleosts, the clade I enzyme inherited the activity of the ancestral enzyme of swelling the egg envelope by cleavage of the N-terminal region of egg envelope proteins. The clade II enzyme gained two specific cleavage sites, N-ZPd and mid-ZPd but lost the ancestral activity. Thus, euteleostean clade II enzymes assumed a new function; solubilization of the egg envelope by the cooperative action with clade I enzyme. However, in Otocephala, the clade II gene was lost during evolution. Consequently, in a late group of Otocephala, only the clade I enzyme is present to swell the egg envelope. We evaluated the egg envelope digestion properties of clade I and II enzymes in Gonorynchiformes, an early diverging group of Otocephala, using milkfish, and compared their digestion with those of other fishes. Finally, we propose a hypothesis of the neofunctionalization process.ResultsThe milkfish clade II enzyme cleaved N-ZPd but not mid-ZPd, and did not cause solubilization of the egg envelope. We conclude that neofunctionalization is incomplete in the otocephalan clade II enzymes. Comparison of clade I and clade II enzyme characteristics implies that the specificity of the clade II enzymes gradually changed during evolution after the duplication event, and that a change in substrate was required for the addition of the mid-ZPd site and loss of activity at the N-terminal region.ConclusionsWe infer the process of neofunctionalization of the clade II enzyme after duplication of the gene. The ancestral clade II gene gained N-ZPd cleavage activity in the common ancestral lineage of the Euteleostei and Otocephala. Subsequently, acquisition of cleavage activity at the mid-ZPd site and loss of cleavage activity in the N-terminal region occurred during the evolution of Euteleostei, but not of Otocephala. The clade II enzyme provides an example of the development of a neofunctional gene for which the substrate, the egg envelope protein, has adapted to a gradual change in the specificity of the corresponding enzyme.

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Genes Encoding Teleost Fish Ligands and Associated Receptors Remained in Duplicate More Frequently than the Rest of the Genome.

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