Structural and functional differentiation of a fat body-like tissue adhering to testis follicles facilitates spermatogenesis in locusts

The fat body is distributed throughout the body of insects, playing the essential role in intermediary metabolism and nutrient storage. However, the function of differentiation of fat bodies adhering to different tissues remains largely unknown. Here, we identified a fat body-like tissue (FLT) surrounding testis follicles and described its features at morphological, cellular and molecular levels. The FLT is morphologically distinguished with the abdominal fat body (FB) and dominated by diploid cells instead of polyploid cells. The transcriptomic analysis demonstrated that the FLT and FB have dramatically different gene expression profiles. Moreover, genes in the cell cycle pathway, which include both DNA replication- and cell division-related genes, were successively active during development of the FLT, suggesting that FLT cells possibly undergo a mitotic cycle rather than an endocycle. Deprivation of the FLT resulted in distortion of the testis follicles, disappearance of sperm bundles, reduction of total sperm number and increase of dead sperm, indicating a critical role of the FLT in the spermatogenesis in testis follicles. The special functional differentiation of the two similar tissues suggested that FLT-FB cells are able to establish a promising system to study mitotic-to-endocycle transition.