Abstract
Ecdysteroids are the hormones regulating development, physiology and fertility in arthropods, which synthesize them exclusively from dietary sterols. But how dietary sterol diversity influences the ecdysteroid profile, how animals ensure the production of desired hormones and whether there are functional differences between different ecdysteroids produced in vivo remains unknown. This is because currently there is no analytical technology for unbiased, comprehensive and quantitative assessment of the full complement of endogenous ecdysteroids. We developed a new LC-MS/MS method to screen the entire chemical space of ecdysteroid-related structures and to quantify known and newly discovered hormones and their catabolites. We quantified the ecdysteroidome in Drosophila melanogaster and investigated how the ecdysteroid profile varies with diet and development. We show that Drosophila can produce four different classes of ecdysteroids, which are obligatorily derived from four types of dietary sterol precursors. Drosophila makes makisterone A from plant sterols and epi-makisterone A from ergosterol, the major yeast sterol. However, they prefer to selectively utilize scarce ergosterol precursors to make a novel hormone 24,28-dehydromakisterone A and trace cholesterol to synthesize 20-hydroxyecdysone. Interestingly, epi-makisterone A supports only larval development, whereas all other ecdysteroids allow full adult development. We suggest that evolutionary pressure against producing epi-C-24 ecdysteroids might explain selective utilization of ergosterol precursors and the puzzling preference for cholesterol.
Highlights
Drosophila melanogaster is emerging as a powerful model in which to study hormonal control of growth, metabolism and development
Losses of endogenous ecdysteroids were below 30% and could be normalized by adding an internal standard, muristerone A (MuA), prior to their methanol extraction (Fig. S1B)
To identify ecdysteroids, including any previously unsuspected molecules, we compiled a list of 52 masses of putative molecules that could be derived by 11 common chemical modifications of the six core ecdysteroid structures: 20E, makisterone A (MaA), makisterone C (MaC) (Feldlaufer et al, 1991; Mauchamp et al, 1993) and their non-hydroxylated precursors (Table S1)
Summary
Drosophila melanogaster is emerging as a powerful model in which to study hormonal control of growth, metabolism and development (reviewed by Padmanabha and Baker, 2014; Shim et al, 2013; Tennessen and Thummel, 2011). Ecdysteroids – the steroid hormones of arthropods – are key regulators of a network of interorgan communication that triggers molting and regulates growth, Received 1 April 2015; Accepted 3 September 2015 metabolism and fertility (reviewed by Lafont et al, 2012). Ecdysteroids are synthesized from sterols in the prothoracic gland as pro-hormones and are further activated by C-20 hydroxylation in the intestine and fat body (Petryk et al, 2003). Control of ecdysteroid biosynthesis in the prothoracic gland clearly plays a key role and is regulated by signals from multiple tissues. Several ecdysteroids common to other insects have been identified in Drosophila (Blais et al, 2010; Bownes et al, 1984) but it is unclear whether the list is exhaustive and how it depends on the developmental stage and diet (Feldlaufer et al, 1995)
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