Translocation of promoter-conserved hatching enzyme genes with intron-loss provides a new insight in the role of retrocopy during teleostean evolution

Abstract

The hatcing enzyme gene ( HE ) encodes a protease that is indispensable for the hatching process and is conserved during vertebrate evolution. During teleostean evolution, it is known that HE experienced a drastic transfiguration of gene structure, namely, losing all of its introns. However, these facts are contradiction with each other, since intron-less genes typically lose their original promoter because of duplication via mature mRNA, called retrocopy. Here, using a comparative genomic assay, we showed that HEs have changed their genomic location several times, with the evolutionary timings of these translocations being identical to those of intron-loss. We further showed that HEs maintain the promoter sequence upstream of them after translocation. Therefore, teleostean HE s are unique genes which have changed intra- (exon-intron) and extra-genomic structure (genomic loci) several times, although their indispensability for the reproductive process of hatching implies that HE genes are translocated by retrocopy with their promoter sequence.

Genomic and phylogenetic analysis of choriolysins, and biological activity of hatching liquid in the flatfish Senegalese sole

“…Choriolysin-encoding genes are routinely classified into two main clades, referred to as I and II that act cooperatively for the stepwise cleavage of the egg envelope proteins. While enzymes in clade I swells the envelope, the clade II choriolysins fully solubilize the chorion and release the larvae [5, 7]. In this study, two type I HCE genes tandemly arrayed in separate multicopy clusters and two type-II enzymes, named HE and LCE, were identified.…”

“…The tight control of these developmental stages for larval survival exerts a high evolutionary pressure on their functional domains resulting in a high conservation in teleost lineage [1, 3]. In spite of these functional evolutionary restrictions, choriolysin-encoding genes irradiated in the fish genomes as an adaptive mechanism to different environments that can be present in a variable number of copies in some species as the result of two major forces: the genome duplication that occurred in teleost lineage and the retrocopy and translocation events that modified the intron-exon structure and genome organization [5, 7, 35, 36]. In the flatfish S .…”

“…Lack of introns and tandemly arrangement in the genome is a common feature for HCE genes in euteleostei. These characteristics are mainly explained by a retrocopy origin in which the new genes maintained the upstream promoters and rearranged through the genome in functional multicopy arrays [7, 35]. Although the HCE clusters moved at least twice in fish genomes and synteny is conserved in euteleostei [7], a further reorganization seemed to occur in the flatfish lineage to create two separate gene clusters (referred to as HCEa and HCEb).…”

“…These characteristics are mainly explained by a retrocopy origin in which the new genes maintained the upstream promoters and rearranged through the genome in functional multicopy arrays [7, 35]. Although the HCE clusters moved at least twice in fish genomes and synteny is conserved in euteleostei [7], a further reorganization seemed to occur in the flatfish lineage to create two separate gene clusters (referred to as HCEa and HCEb). Although HCEa and HCEb open reading frames were highly similar, some divergence was observed in the non-coding 3'-UTR that indicating that these gene rearrangements occured recently although currently they could be not evolving concertedly.…”

Effects of hatching enzymes on egg envelope digestion in the male‐brooding seahorse

“…Furthermore, exon‐intron structures of the hatching enzyme genes are also conserved with other euteleosts, that is, seahorse HCE is intron‐less, while seahorse LCE gene is composed of eight exons. It is reported that synteny of the LCE gene is well conserved among euteleostean fishes, while the HCE gene (without introns) is translocated frequently by retrocopying (Nagasawa et al, 2019). At the time retrocopying, not only HCE gene but also the conserved promoter sequence translocated together, and therefore, HCE gene is actively expressed in teleosts (Nagasawa et al, 2019).…”