Seasonal changes of mitochondrial autophagy and oxidative response in the testis of the wild ground squirrels (Spermophilus dauricus)

Mitochondria are the main organelles for mammalian energy metabolism and have been implicated in the regulation of germ cell maintenance and spermatogenesis. However, little is known about the changes in the mitochondria of the testis of seasonal breeders. Here, we characterized the seasonal changes in the mitochondria in the testis of the wild ground squirrels. Increased testicle weight, seminiferous tubule diameter, and sperm count were observed in the wild ground squirrels at the breeding season. RNA-seq analysis of the wild ground squirrel testes revealed that mitochondrial-related genes were expressed differentially between the breeding and nonbreeding seasons. Immunohistochemical staining showed that key mitophagy factors including PINK1, MFN2, and PARKIN were highly expressed in various cell types of testis during the breeding season. In addition, the abundance and enzymatic activities of mitochondrial-localized antioxidative enzymes superoxide dismutase 2 (SOD2) and Catalase were decreased in the testis during the breeding season, suggesting a tightly controlled redox balance at least partially facilitated by mitophagy during the seasonal breeding. Taken together, our study reveals that mitochondrial autophagy and oxidative stress may be implicated in the seasonal reproductive recrudescence of the wild ground squirrels, which deepens our understanding of the mitochondrial regulation of seasonal reproductivity in wildlife and provides new insights into the development of potential therapeutic interventions of male infertility.

Automated summary

By studying the seasonal changes in mitochondria in the testis of wild ground squirrels, it was found that mitochondrial autophagy and oxidative stress may be involved in the regulation of seasonal reproduction; during the breeding season, mitochondrial-related genes were differentially expressed, key mitophagy factors were highly expressed, and the abundance and enzymatic activities of antioxidative enzymes were decreased, indicating an important role of mitochondria in seasonal reproduction.