Body-Fat Sensor Triggers Ribosome Maturation in the Steroidogenic Gland to Initiate Sexual Maturation in <i>Drosophila</i>

Abstract

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.