Evolution of hes gene family in vertebrates: the hes5 cluster genes have specifically increased in frogs

Aya Kuretani,Masanori Taira,Tatsuo Michiue,Takayoshi Yamamoto

doi:10.1186/s12862-021-01879-6

Aya Kuretani, Masanori Taira + Show 2 more

Open Access

https://doi.org/10.1186/s12862-021-01879-6

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Abstract

Backgroundhes genes are chordate homologs of Drosophila genes, hairy and enhancer of split, which encode a basic helix-loop-helix (bHLH) transcriptional repressor with a WRPW motif. Various developmental functions of hes genes, including early embryogenesis and neurogenesis, have been elucidated in vertebrates. However, their orthologous relationships remain unclear partly because of less conservation of relatively short amino acid sequences, the fact that the genome was not analyzed as it is today, and species-specific genome duplication. This results in complicated gene names in vertebrates, which are not consistent in orthologs. We previously revealed that Xenopus frogs have two clusters of hes5, named “the hes5.1 cluster” and “the hes5.3 cluster”, but the origin and the conservation have not yet been revealed.ResultsHere, we elucidated the orthologous and paralogous relationships of all hes genes of human, mouse, chicken, gecko, zebrafish, medaka, coelacanth, spotted gar, elephant shark and three species of frogs, Xenopus tropicalis (X. tropicalis), X. laevis, Nanorana parkeri, by phylogenetic and synteny analyses. Any duplicated hes5 were not found in mammals, whereas hes5 clusters in teleost were conserved although not as many genes as the three frog species. In addition, hes5 cluster-like structure was found in the elephant shark genome, but not found in cyclostomata.ConclusionThese data suggest that the hes5 cluster existed in the gnathostome ancestor but became a single gene in mammals. The number of hes5 cluster genes were specifically large in frogs.

Highlights

To determine when the hes5 clusters emerged, we first performed a phylogenetic analysis of sarcopterygian hes5 genes (Fig. 1, Additional file 1: Fig. S2; complete tree was shown in Additional file 1: Fig. S4)
Maximum likelihood (ML) phylogenetic tree construction revealed that all the hes5 genes we examined were assigned in a single clade with a high bootstrap value (Fig. 1A)
We estimated the evolutionary origins of the two hes5 clusters, which have been found in Xenopus

Summary

Results

Classification of hes genes in sarcopterygian Our previous studies on the identification of hes genes have shown that there are ten hes paralogs in X. laevis, which we refer to as "the hes5.1 cluster" or "the hes5.3 cluster" [11]. Classification of hes genes in gnathostomata To determine the origin of the hes cluster, we carried out phylogenetic analysis with spotted gar (Lepisosteus oculatus), elephant shark (Callorhinchus milii), lamprey (Petromyzon marinus), and amphioxus (Branchiostoma floridae) (Fig. 5A, B, Additional file 1: Fig. S3; the complete tree is shown in Additional file 1: Fig. S6). Many hes5-like genes were found to be clustered on the genomes: two hes5-like genes were located next to pank, and six hes5-like genes were located between nol and zbtb ( TAS1R1 was inserted into the hes gene cluster locus, which was not found around the hes5.1 or hes5.3 cluster in Xenopus) (Fig. 8A) These results suggest that the two hes genes on Scaffold815 of Tibetan frog are classified to the hes5.1 cluster and the other six genes on Scaffold are to the hes5.3 cluster.

Conclusion

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Conclusions

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