Sexually Dimorphic Gene Expression in X and Y Sperms Instructs Sexual Dimorphism of Embryonic Genome Activation in Yellow Catfish (Pelteobagrus fulvidraco)

SIMPLE SUMMARY: After fertilization, maternal degradation, zygotic activation, and paternal activation are three major activities during early embryonic development. Genes involved in these activities are assumed to contribute to sex determination and sexual dimorphism. To our knowledge, paternal genes are activated along with zygotic gene activation, but the influence of paternal inheritance on sex determination and sexual dimorphism is still unclear. As a potential model, yellow catfish (Pelteobagrus fulvidraco) is sexually dimorphic in growth rate with males growing faster than females. We performed sex-control breeding of this fish and successfully created XX neo-male and YY super-males by sex reversal technology, which provided purified X and Y spermatozoa for paternal genetic research. Studies of gene expression and DNA methylation of spermatozoa indicated a big proportion of upregulated genes in Y sperm with slightly lower DNA methylation levels. Maternal-to-zygotic transition (MZT) processes were identified from the XX female and XY male offspring through a combined analysis of SNP and transcriptomic dynamics, demonstrating the low-blastocyst stage as a critical time point of zygotic and paternal activation. The emergence of sex differences lagged behind gene expression differences. Integration analysis of X/Y sperm and embryos revealed the influence of paternal inheritance on sexual dimorphism of genome activation. ABSTRACT: Paternal factors play an important role in embryonic morphogenesis and contribute to sexual dimorphism in development. To assess the effect of paternal DNA on sexual dimorphism of embryonic genome activation, we compared X and Y sperm and different sexes of embryos before sex determination. Through transcriptome sequencing (RNA-seq) and whole-genome bisulfite sequencing (WGBS) of X and Y sperm, we found a big proportion of upregulated genes in Y sperm, supported by the observation that genome-wide DNA methylation level is slightly lower than in X sperm. Cytokine–cytokine receptor interaction, TGF-beta, and toll-like receptor pathways play important roles in spermatogenesis. Through whole-genome re-sequencing (WGRS) of parental fish and RNA-seq of five early embryonic stages, we found the low-blastocyst time point is a key to maternal transcriptome degradation and zygotic genome activation. Generally, sexual differences emerged from the bud stage. Moreover, through integrated analysis of paternal SNPs and gene expression, we evaluated the influence of paternal inheritance on sexual dimorphism of genome activation. Besides, we screened out gata6 and ddx5 as potential instructors for early sex determination and gonad development in yellow catfish. This work is meaningful for revealing the molecular mechanisms of sex determination and sexual dimorphism of fish species.