Evolutionary significance and regulated expression of Tdrd family genes in gynogenetic Japanese flounder (Paralichthys olivaceus)

Abstract

Tudor domain-containing proteins (TDRDs) are highly conserved among organisms and have a function in gonads to regulate gametogenesis and genome stability through the piwi-interacting RNA (piRNA) pathway. With diverse sexual development patterns in teleost species, the evolution and function of Tdrd genes among teleosts remain unclear. Here, we identified and characterized 12 Tdrd genes (PoTdrds) in Japanese flounder (Paralichthys olivaceus) which represents dramatic sexual dimorphic metrics and sex reversal during sex differentiation. Phylogenetic and comparative synteny indicated the gain and loss of Tdrd genes after teleost-specific whole-genome duplication (3R-WGD). Tdrd1, Tdrd5, Tdrd6 and Ecat8 were abundantly expressed in their gonads. Four PoTdrds (Tdrd6, Tdrd7b, Tdrd9 and Ecat8) represented significant male-biased expression in gynogenetic and wild-type Japanese flounder gonads (p < .01). This finding indicated their important roles in spermatogenesis of P. olivaceus. Some PoTdrds were either highly up-regulated in gynogenetic testis (Tdrd3, Tdrd5, Tdrd7b and Ecat8) or down-regulated in gynogenetic ovary (Tdrkh, Tdrd3, Tdrd6l) compared with wild-type gonads (p < .05). Molecular evolution tests revealed that the selective pressure of Tdrd6/6l differed between ancestral aquatic and terrestrial organisms with 13 positively selected sites found in the ancestral lineages of teleost Tdrd6. Expression profile analysis suggested that PoTdrd6 differed significantly from PoTdrd6l, indicating sub-functionalization after 3R-WGD. All these results are important for the functional annotation of Tdrd genes and can benefit the further deciphering of Tdrd functions during gonadal development and gametogenesis of teleost fish.