The evolutionary foundation of genomic imprinting in lower vertebrates

In mammals, genomic imprinting confers developmental asymmetry and complementation on the parental genomes and makes both parental genomes essential for complete development. Genomic imprinting is, therefore, the first regulatory step of genome-wide gene expression of embryogenesis and thought to be the epigenetic foundation of bisexual reproduction. However, how the genomic imprinting is originated, established and maintained during vertebrate evolution remains unknown. Because no endogenous imprinting gene has been identified in non-mammalian vertebrates, genomic imprinting is thought to be a unique evolutionary event of mammals. Here, in order to study the evolutionary origin of genomic imprinting in vertebrates, we examined whether parent-specific methylation occurred in the teleost homologue of mammalian imprinting gene during gametogenesis. Bisulfate sequencing analysis showed that, as mammalian Igf2 CpG island, goldfish Igf2 CpG island was a parental differentially methylated region (DMR) that was hypermethylated in sperm but unmethylated in eggs. Unlike mammalian imprinting gene DMR, however, the parent-specific methylation pattern of goldfish Igf2 DMR was not maintained during embryogenesis, suggesting that the parent-specific methylation of goldfish Igf2 DMR might be a primitive genomic imprinting in the early period of vertebrate evolution. These results indicate that the evolutionary foundation of genomic imprinting exists in lower vertebrates and genomic imprinting should not be considered as a unique evolutionary event of mammals.