Intron-loss evolution of hatching enzyme genes in Teleostei

Abstract

BackgroundHatching enzyme, belonging to the astacin metallo-protease family, digests egg envelope at embryo hatching. Orthologous genes of the enzyme are found in all vertebrate genomes. Recently, we found that exon-intron structures of the genes were conserved among tetrapods, while the genes of teleosts frequently lost their introns. Occurrence of such intron losses in teleostean hatching enzyme genes is an uncommon evolutionary event, as most eukaryotic genes are generally known to be interrupted by introns and the intron insertion sites are conserved from species to species. Here, we report on extensive studies of the exon-intron structures of teleostean hatching enzyme genes for insight into how and why introns were lost during evolution.ResultsWe investigated the evolutionary pathway of intron-losses in hatching enzyme genes of 27 species of Teleostei. Hatching enzyme genes of basal teleosts are of only one type, which conserves the 9-exon-8-intron structure of an assumed ancestor. On the other hand, otocephalans and euteleosts possess two types of hatching enzyme genes, suggesting a gene duplication event in the common ancestor of otocephalans and euteleosts. The duplicated genes were classified into two clades, clades I and II, based on phylogenetic analysis. In otocephalans and euteleosts, clade I genes developed a phylogeny-specific structure, such as an 8-exon-7-intron, 5-exon-4-intron, 4-exon-3-intron or intron-less structure. In contrast to the clade I genes, the structures of clade II genes were relatively stable in their configuration, and were similar to that of the ancestral genes. Expression analyses revealed that hatching enzyme genes were high-expression genes, when compared to that of housekeeping genes. When expression levels were compared between clade I and II genes, clade I genes tends to be expressed more highly than clade II genes.ConclusionsHatching enzyme genes evolved to lose their introns, and the intron-loss events occurred at the specific points of teleostean phylogeny. We propose that the high-expression hatching enzyme genes frequently lost their introns during the evolution of teleosts, while the low-expression genes maintained the exon-intron structure of the ancestral gene.

An evolutionary insight into the hatching strategies of pipefish and seahorse embryos

“…B). Both genes were comprised of eight exons interrupted by seven introns, whose structure, including intron insertion sites and intron phases, conserved those of other euteleostean LCE genes (Kawaguchi et al, ).…”

“…The hatching enzymes, HCE and LCE, are astacin family proteases, and possess two active site consensus sequences conserved within the family (Bond and Beynon, ). The degenerate primers designed from the consensus sequences (Kawaguchi et al, ) were used to amplify both HCE and LCE cDNAs from two pipefishes by RT‐PCR. The cloned HCE and LCE cDNAs were identified from the amino acid sequence similarity to other euteleostean HCE and LCE, respectively, and were named using the specific name of each species, that is, the genes for alligator pipefish S. biaculeatus were abbreviated to SbHCE and SbLCE, respectively.…”

Comparison of Egg Envelope Thickness in Teleosts and its Relationship to the Sites of ZP Protein Synthesis

“…The evolution of teleost ZP genes, focusing on the organ expressing the ZP genes, is as follows: Elopomorpha, to which Japanese eel Anguilla japonica belongs, express ZP genes and synthesize ZP proteins in oocytes (Sano et al., ). Subsequently, liver‐expressed ZP genes were produced by duplication and diversification in a common ancestor of Euteleostei and Otocephala (Kawaguchi et al., , ). All euteleost fish and Clupeiformes, which is diverged early from Otocephala, have both ovarian‐ and liver‐expressing ZP genes (Sano et al., ).…”

Neofunctionalization of a duplicate hatching enzyme gene during the evolution of teleost fishes

“…In teleosts, we have cloned 67 hatching enzyme genes from 27 species, and elucidated their evolutionary pathway [14,15]. The majority of fishes have several hatching enzyme genes in their genomes, suggesting that there were several duplication events of hatching enzyme genes during evolution of the fish lineage [16].…”