Abstract
Apoptosis is a tightly controlled process by which tissues eliminate unwanted cells. Spontaneous germ cell apoptosis in testis has been broadly investigated in mammals that have an associated spermatogenesis pattern. However, the mechanism of germ cell apoptosis in seasonally breeding reptiles following a dissociated spermatogenesis has remained enigmatic. In the present study, morphological evidence has clearly confirmed the dissociated spermatogenesis pattern in Pelodiscus sinensis. TUNEL and TEM analyses presented dynamic changes and ultrastructural characteristics of apoptotic germ cells during seasonal spermatogenesis, implying that apoptosis might be one of the key mechanisms to clear degraded germ cells. Furthermore, using RNA-Seq and digital gene expression (DGE) profiling, a large number of apoptosis-related differentially expressed genes (DEGs) at different phases of spermatogenesis were identified and characterized in the testis. DGE and RT-qPCR analysis revealed that the critical anti-apoptosis genes, such as Bcl-2, BAG1, and BAG5, showed up-regulated patterns during intermediate and late spermatogenesis. Moreover, the increases in mitochondrial transmembrane potential in July and October were detected by JC-1 staining. Notably, the low protein levels of pro-apoptotic cleaved caspase-3 and CytC in cytoplasm were detected by immunohistochemistry and western blot analyses, indicating that the CytC-Caspase model might be responsible for the effects of germ cell apoptosis on seasonal spermatogenesis. These results facilitate understanding the regulatory mechanisms of apoptosis during spermatogenesis and uncovering the biological process of the dissociated spermatogenesis system in reptiles.
Highlights
Spermatogenesis is a highly organized and complex process that is divided into the mitotic division of spermatogonia, spermatocytic meiosis and the production of mature spermatozoa in the testes of male vertebrates (de Kretser et al, 1998)
In the testes of P. sinensis, the seminiferous tubules are lined along the seminiferous epithelium, which rested on a basement membrane and surrounded a centrally located lumen
Spermatogenesis within the Chinese soft-shelled turtle (Pelodiscus sinensis) is closely parallel to that seen in most temperate and boreal reptilian species (Rheubert et al, 2009b; Sousa et al, 2014)
Summary
Spermatogenesis is a highly organized and complex process that is divided into the mitotic division of spermatogonia, spermatocytic meiosis and the production of mature spermatozoa in the testes of male vertebrates (de Kretser et al, 1998). In some seasonally breeding reptilian species, Apoptosis in Dissociated Spermatogenesis spermatogenesis is highly seasonal and not coupled in time with male mating behavior, which is called a dissociated reproductive pattern (Gribbins et al, 2006; Rheubert et al, 2009a; Clesson et al, 2013). These reptiles have germ cell cohorts that develop together as a population and are typically released into centralized lumina in one unified spermiation event at the end of spermatogenesis. The dissociated spermatogenesis system has been widely described and the transitional and evolutionarily significance has been reported in many turtle species, the mechanisms underlying dissociated spermatogenesis have not been fully elucidated
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