Fat stores are critical for reproductive success and may govern maturation initiation. Here, we report that signaling and sensing fat sufficiency for sexual maturation commitment requires the lipid carrier apolipophorin in fat cells and Sema1a in the neuroendocrine prothoracic gland (PG). Larvae lacking apolpp or Sema1a fail to initiate maturation despite accruing sufficient fat stores, and they continue gaining weight until death. Mechanistically, sensing peripheral body-fat levels via the apolipophorin/Sema1a axis regulates endocytosis, endoplasmic reticulum remodeling, and ribosomal maturation for the acquisition of the PG cells' high biosynthetic and secretory capacity. Downstream of apolipophorin/Sema1a, leptin-like upd2 triggers the cessation of feeding and initiates sexual maturation. Human Leptin in the insect PG substitutes for upd2, preventing obesity and triggering maturation downstream of Sema1a. These data show how peripheral fat levels regulate the control of the maturation decision-making process via remodeling of endomembranes and ribosomal biogenesis in gland cells.
Fat stores are critical for reproductive success and may govern maturation initiation. Here, we report that the prothoracic gland in Drosophila larvae monitors peripheral fat for sexual maturation commitment via semaphorin 1a (Sema1a). Larvae with prothoracic gland knockdown of Sema1a do not mature, and continue to grow excessively. The same phenotype occurs after reducing the lipid carrier ApoB/lipophorin in the fat body. Super-resolution imaging revealed that at critical weight, an endoplasmic reticulum trafficking signal is released that permits protein transport to the membrane and secretion and stimulates ribosomal biogenesis. Downstream of the Sema1a sensor, the leptin-like hormone upd2 signals critical weight attainment to the body, leading to events that initiate sexual maturation. These data show how peripheral fat regulates maturation decision-making and reveal the fundamental roles of semaphorin and of ribosome maturation and translation in cellular trafficking.
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