Deciphering teleost testis development throughout the annual cycle: Insights from transcriptomic features and thyroid hormone signaling pathway.

Abstract

Testis development and spermatogenesis in adult teleosts are seasonally regulated throughout the annual reproductive cycle, with notable changes occurring in cellular composition and molecular characteristics. However, the molecular mechanisms underlying this process are not fully understood. In this study, a landscape integrating histological and molecular features of S. schlegelii testis development throughout the annual reproductive cycle was constructed. It was found that the transition from the Rg stage to the E_Dif stage represents a critical period in the annual reproductive cycle of S. schlegelii, involving key biological processes and signaling pathways, such as the cell cycle, microtubule dynamics, and thyroid hormone regulation. Furthermore, thyroid hormone T3 was shown to expedite germ cell meiosis and cell cycle progression, thereby accelerating testis development. The thyroid hormone receptor thrb, which is highly expressed in testicular germ cells, was found to regulate the transcription of cell cycle genes and influence the expression of meiotic genes. Finally, protein interaction between THRB and two other germ cell-enriched transcription factors, RXRBA and RXRBB, was confirmed. In summary, our study provides a comprehensive molecular understanding of the annual cycle development of teleost testis, which may be beneficial for regulating testicular development and spermatogenesis in aquaculture.