Origin, evolution, and tissue-specific functions of the porcine repetitive element 1

BACKGROUND: The porcine repetitive element 1 (PRE1) is the most abundant short interspersed nuclear element (SINE) in the Sus scrofa genome and it has been suggested that some PRE1 can have regulatory functions. The million copies of PRE1 in the porcine genome have accumulated abundant CpG dinucleotides and unique structural variations, such as direct repeats and patterns of sequence degeneration. The aims of this study were to analyse these structural variations to trace the origin and evolutionary pattern of PRE1 and to investigate potential methylation-related functions of PRE1 based on methylation patterns of PRE1 CpG dinucleotides in different tissues. RESULTS: We investigated the evolutionary trajectory of PRE1 and found that PRE1 originated from the ancestral CHRS-S1 family through three main successive partial duplications. We found that the partial duplications and deletions of PRE1 were likely due to RNA splicing events during retrotransposition. Functionally, correlation analysis showed that the methylation levels of 103 and 261 proximal PRE1 were, respectively, negatively and positively correlated with the expression levels of neighboring genes (Spearman correlation, P < 0.01). Further epigenomic analysis revealed that, in the testis, demethylation of proximal PRE1 in the HORMAD1 and HACD3 genes had tissue-specific enhancer and promoter functions, while in the muscle, methylation of proximal PRE1 repeats in the TCEA3 gene had an enhancer function. CONCLUSIONS: The characteristic sequences of PRE1 reflect unique patterns of origin and evolution and provide a structural basis for diverse regulatory functions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12711-022-00745-3.