Molecular evolution of hatching enzymes and their paralogous genes in vertebrates.

Hatching is identified as one of the most important events in the reproduction of oviparous vertebrates. The genes for hatching enzymes, which are vital in the hatching process, are conserved among vertebrates. However, especially in teleost, it is difficult to trace their molecular evolution in detail due to the presence of other C6astacins, which are the subfamily to which the genes for hatching enzymes belong and are highly diverged. In particular, the hatching enzyme genes are diversified with frequent genome translocations due to retrocopy. In this study, we took advantage of the rapid expansion of whole-genome data in recent years to examine the molecular evolutionary process of these genes in vertebrates. The phylogenetic analysis and the genomic synteny analysis revealed C6astacin genes other than the hatching enzyme genes, which was previously considered to be retained only in teleosts, was also retained in the genomes of basal ray-finned fishes, coelacanths, and cartilaginous fishes. These results suggest that the common ancestor of these genes can be traced back to at least the common ancestor of the Gnathostomata. Moreover, we also found that many of the C6astacin genes underwent multiple gene duplications during vertebrate evolution, and the results of gene expression analysis in frogs implied that genes derived from hatching enzyme genes underwent neo-functionalization. In this study, we describe in detail the molecular evolution of the C6astacin gene in vertebrates, which has not been summarized previously. The results revealed the presence of the previously unknown C6astacin gene in the basal-lineage of jawed vertebrates and large-scale gene duplication of hatching enzyme genes in amphibians. The comprehensive investigation reported in this study will be an important basis for studying the molecular evolution of the vertebrate C6astacin genes, hatching enzyme, and its paralogous genes and for identifying these genes without the need for gene expression and functional analysis. The online version contains supplementary material available at 10.1186/s12862-022-01966-2.

孵化被认为是卵生脊椎动物繁殖过程中最重要的事件之一。孵化酶基因在孵化过程中至关重要，在脊椎动物中是保守的。然而，特别是在硬骨鱼中，由于存在其他C6astacins（孵化酶基因所属的亚家族，且高度分化），很难详细追踪它们的分子进化。特别是，由于反转录复制，孵化酶基因因频繁的基因组易位而多样化。 在这项研究中，我们利用近年来全基因组数据的快速增长来研究这些基因在脊椎动物中的分子进化过程。系统发育分析和基因组同线性分析显示，除孵化酶基因外的C6astacin基因（此前被认为仅保留在硬骨鱼中）也保留在基部辐鳍鱼、腔棘鱼和软骨鱼的基因组中。这些结果表明，这些基因的共同祖先至少可以追溯到有颌类的共同祖先。此外，我们还发现许多C6astacin基因在脊椎动物进化过程中经历了多次基因复制，并且青蛙的基因表达分析结果表明，源自孵化酶基因的基因经历了新功能化。 在这项研究中，我们详细描述了脊椎动物中C6astacin基因的分子进化，这在此前尚未被总结。结果揭示了在有颌脊椎动物基部谱系中存在此前未知的C6astacin基因，以及两栖动物中孵化酶基因的大规模基因复制。本研究报告的综合调查将是研究脊椎动物C6astacin基因、孵化酶及其旁系同源基因的分子进化以及无需基因表达和功能分析即可识别这些基因的重要基础。 网络版包含补充材料，可在10.1186/s12862 - 022 - 01966 - 2获取。