Mating-induced increase of kynurenine in Drosophila ovary enhances starvation resistance of progeny

Abstract

The maternal nutritional environment can impact progeny development, stress tolerance, and longevity. Such phenotypic variation of offspring resulting from the maternal environment is often referred to as the 'maternal effect' and is observed across taxa, including in humans. While some mechanisms behind maternal effects have been revealed, such as histone modification, many studies rely on drastic genetic or nutritional manipulation in describing these mechanisms. Here we aimed to reveal how the maternal environment is regulated under physiological conditions to affect the progeny. Specifically, we detailed metabolic regulation in oocytes in response to mating using Drosophila melanogaster fruit flies. Using liquid chromatography–mass spectrometry (LC-MS), we found that upon mating, the ovary metabolites shifted, predominantly toward increasing amino acids (AAs) and the tryptophan/kynurenine (Trp/Kyn) pathway. This mating-induced increase in ovary Kyn was driven by increased Kyn production in the fat body (FB), a functional counterpart of the mammalian liver and white adipose tissue, and the source of Kyn storage for the ovary after mating. Furthermore, we show maternal Kyn repression decreased the starvation resistance of progeny, and that administering exogenous Kyn to the maternal generation enhanced the starvation resistance of female progeny. Taken together, these findings point to a previously unidentified role of FB Kyn distribution during reproduction on progeny survival.