Evolutionary dynamics and conserved function of the Tudor domain-containing (TDRD) proteins in teleost fish

Abstract

Tudor domain-containing (TDRD) proteins, the germline enriched protein family, play essential roles in the process of gametogenesis and genome stability through their interaction with the PIWI-interacting RNA (piRNA) pathway. Several studies have suggested the rapid evolution of the piRNA pathway in teleost lineages with striking reproductive diversity. However, there is still limited information about the function and evolution of Tdrd genes in teleost species. In this study, through genome wide screening, 13 Tdrd family genes were identified in economically important aquaculture fish, including spotted sea bass (Lateolabrax maculatus), Asian sea bass (Lates calcarifer), and tongue sole (Cynoglossus semilaevis). With copy number, structure, phylogeny, and synteny analysis, duplication of Tdrd6 and Tdrd7, as well as loss of Stk31 and Tdrd10, were characterized in teleost lineages. Codon based molecular evolution analysis indicated faster evolution of teleost Tdrd genes than that in mammals, potentially associated with the accelerated evolution of the piRNA pathway in teleost lineages. The evolutionary diversity of Tdrd genes was also detected between different teleost lineages. RNA-seq analysis showed that most teleost Tdrd genes were dominantly expressed in gonads, particularly highly expressed in testis, such as Tdrd6, Tdrd7a, Tdrd9, Ecat8, and Tdrd15. The varied expression and evolutionary pattern between the duplicated Tdrd6 and Tdrd7 in teleosts may indicate their functional diversification. All these results suggest a conserved function of teleost Tdrd family in gametogenesis and the piRNA pathway, which could lay a foundation for the evolution of Tdrd genes and be helpful for further deciphering of Tdrd functions in teleosts.