Long-read genome assemblies reveals acis-regulatory landscape associated with phenotypic divergence in two sisterSinipercafishes

AbstractBackgroundDissecting the genetic basis of variation in the regulation of gene expression is essential for understanding phenotypic evolution. Structural variants intersecting thecis-regulatory elements are found to cause gene expression variation in several developmental genes, resulting in morphological divergence between species. Due to the difficulty of identifying structural variants accurately across the genome, a comprehensive study of impacts of structural variants incis-regulatory divergence of closely related species, especially fish species, is still scarce. Recently identified broad H3K4me3 domains are essential for the regulation of genes involved in several biological processes. However, the role of broad H3K4me3 domains in phenotypic divergence remain poorly understood.Siniperca chuatsiandS. scherzeriare two closely related fish species diverge in several phenotypic traits, making them an ideal model to studycis-regulatory evolution in closely related species.ResultsWe generated chromosome-level genomes ofS. chuatsiandS. scherzeri. The evolutionary histories ofS. chuatsiandS. scherzeriwere studied by inferring the dynamic changes in the ancestral population sizes. The genetic basis of adaptation inS. chuatsiandS. scherzeriwas dissected by performing gene family expansion and contraction analysis and identifying positively selected genes (PSGs). To investigate the role of SVs incis-regulatory divergence of closely related fish species, we identified high-quality SVs betweenS. chuatsiandS. scherzeri, as well as H3K27ac and H3K4me3 domains. Integrated analysis revealed thatcis-regulatory divergence caused by SVs played an essential role in the differentiation of metabolism, skin pigmentation, and immunity betweenS. chuatsiandS. scherzeri. Additionally, divergent broad H3K4me3 domains were found to mostly associate with cancer-related genes inS. chuatsiandS. scherzeriand contribute to their phenotypic divergence.ConclusionsOur analysis reveals SVs play an essential role incis-regulatory variation between the two sister fish species, which in turn contributes to their phenotypic divergence. The divergence of broad H3K4me3 domains contributes to phenotypic divergence between closely related species. Additionally, the association of broad H3K4me3 domains and cancer-related genes has an ancient origin.