Transcriptome analysis of the hypothalamus and testes in Brandt’s Vole: new insights into mechanisms of photoperiodic plasticity in postnatal testicular development

Postnatal gonadal development is regulated by photoperiod via the hypothalamus, especially in seasonal breeding small rodents. However, the precise molecular mechanisms remain unclear. In this study, we conducted a comparative analysis of the transcriptomes of the hypothalamus and testes in 10-week-old male Brandt’s voles born under long (LP, 16L:8D) and short photoperiod (SP, 8L:16D) conditions. Results indicate that the SP group exhibited significantly smaller testes with spermatogenesis halted before meiosis, identifying 129 differentially expressed genes (DEGs) in the hypothalamus and 21,673 DEGs in the testes. In the hypothalamus, genes involved in the thyroid hormone and retinoic acid (RA) pathway were notably altered under SP conditions, including decreased Tshb and Cga expression, increased Dio3, and reduced Crabp1 and Lrat, highlighting their key roles in SP signaling. In the testes, downregulated genes were significantly enriched in male reproduction-related GO terms and metabolic KEGG pathways, such as steroid hormone biosynthesis and retinol metabolism. Key genes for testosterone synthesis (e.g. Star, Cyp11a1) and RA synthesis (e.g. Rdh10, Rdh11) were downregulated, while those linked to RA degradation (Cyp26b1) and undifferentiated spermatogonia maintenance (e.g. Gdnf, Gfra1) were upregulated. These findings outline a molecular microenvironment that favors the preservation of undifferentiated spermatogonia over their differentiation from the hypothalamus to the testes. This study firstly provides valuable insights into the transcriptomic basis of SP-inhibited testicular development in Brandt’s voles.