The retinoic-like juvenile hormone controls the looping of left-right asymmetric organs in Drosophila

Abstract

In vertebrate development, the establishment of left-right asymmetry is essential for sidedness and the directional looping of organs like the heart. Both the nodal pathway and retinoic acid play major and conserved regulatory roles in these processes. We carried out a novel screen in Drosophila to identify mutants that specifically affect the looping of left-right asymmetric organs. We report the isolation of spin, a novel mutant in which the looping of the genitalia and spermiduct are incomplete; under-rotation of the genitalia indicates that spincontrols looping morphogenesis but not direction, thus uncoupling left-right asymmetry and looping morphogenesis. spin is a novel,rotation-specific allele of the fasciclin2 (Fas2) gene,which encodes a cell-adhesion protein involved in several aspects of neurogenesis. In spin mutants, the synapses connecting specific neurosecretory cells to the corpora allata are affected. The corpus allatum is part of the ring gland and is involved in the control of juvenile hormone titers during development. Our genetic and pharmacological results indicate that Fas2spin rotation defects are linked to an abnormal endocrine function and an elevated level of juvenile hormone. As juvenile hormone is an insect sesquiterpenoid related to retinoic acid, these results establish a new genetic model for studying organ looping and demonstrate an evolutionarily conserved role for terpenoids in this process.

Paralogous Genes Involved in Juvenile Hormone Action in Drosophila melanogaster

“…Similarly, treatment of D. melanogaster Met 1 prepupae with JH analogs results in failure of the complete rotation of the male genital disk that normally occurs during pupal development (Adam et al 2003), and Met mutants are completely resistant to this effect (Wilson and Fabian 1986). In our experiments, resistance seen in Met 27 to this methoprene-induced effect was blocked in Met 27 ; UAS-gce/tubulin-GAL4 flies, resulting in abnormal genital rotation, a response similar to that found for Met 1 (Figure 5).…”

Interaction Between Hormonal Signaling Pathways in Drosophila melanogaster as Revealed by Genetic Interaction Between Methoprene-tolerant and Broad-Complex

“…In some cases, this required combining strong mutations with moderate wild-type transgene activity, an established method for revealing late developmental functions (Hall and Thummel 1998). The malrotation phenotype is of particular interest because a genetic interaction between Met and spin, a Fas2 mutation with a malrotation phenotype, has recently been described (Adam et al 2003).…”

A mitochondrial carrier gene, CG32103, is highly expressed in the corpora allata in the fruit fly Drosophila melanogaster (Diptera: Drosophilidae)

“…UAS-GFP.S65T was obtained from the Drosophila Genetic Resource Center at the Kyoto Institute of Technology. AUG21-GAL4, in which the GAL4 transgene is active in CA cells (Siegmund and Korge 2001;Adám et al 2003), was kindly provided from Dr. G. Korge. Double-strand RNA (dsRNA)-mediated RNA interference (RNAi) for CG32103 was performed using the UAS-CG32103-inverted repeat strain P{KK100089} VIE-260B that was obtained from the Vienna Drosophila RNAi Center.…”