Abstract
Metabolism must be coupled with developmental transition to fulfill the energy requirements during an organism's life cycle. In most animals, steroid hormones are crucial regulators of life-stage transitions until adulthood. In the fruit fly Drosophila, ecdysteroid titers drive developmental transitions, such as molting and metamorphosis [1-4]. Although the timings of molting and larval-pupal transition are dependent on environmental and internal conditions, metamorphosis is a temporally controlled life transition event that solely relies on energetic macromolecules accumulated during the larval period. The ecdysteroid signaling cascade and the energetics of metamorphosis have been determined [5-8]. However, the molecular mechanisms that regulate metabolic homeostasis during metamorphosis remain largely unknown. Here, I show that the programmed regulation of carbohydrate metabolism by steroid hormones directs the prepupal-pupal transition in Drosophila. I found that pupation is associated with a transient increase in glucose oxidation. Mechanistically, after pupariation, ecdysteroid signaling and the competence factor Ftz-F1 regulates the systematic degradation of circulating trehalose via the transient induction of trehalose transporters and trehalase (Treh) in a timely manner. Trehalose metabolism is crucial for energy homeostasis at the prepupal-pupal transition. Moreover, trehalose catabolism acts upstream of ecdysteroid biosynthesis and signaling. My findings lead to the hypothesis that trehalose breakdown not only defines energy costs by providing a carbon source but also facilitates pupation by inducing water loss in the puparium. My work sheds light on the ways in which a life-stage transition is driven by the preprogrammed coordination between steroid hormones and catabolism of stored nutrients.
