Myoinhibiting peptides are the ancestral ligands of the promiscuous Drosophila sex peptide receptor
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Male insects change behaviors of female partners by co-transferring accessory gland proteins (Acps) like sex peptide (SP), with their sperm. The Drosophila sex peptide receptor (SPR) is a G protein-coupled receptor expressed in the female’s nervous system and genital tract. While most Acps show a fast rate of evolution, SPRs are highly conserved in insects. We report activation of SPRs by evolutionary conserved myoinhibiting peptides (MIPs). Structural determinants in SP and MIPs responsible for this dual receptor activation are characterized. Drosophila SPR is also expressed in embryonic and larval stages and in the adult male nervous system, whereas SP expression is restricted to the male reproductive system. MIP transcripts occur in male and female central nervous system, possibly acting as endogenous SPR ligands. Evolutionary consequences of the promiscuous nature of SPRs are discussed. MIPs likely function as ancestral ligands of SPRs and could place evolutionary constraints on the MIP/SPR class.
KeywordsAllatostatin GPCR Insect Myoinhibiting peptide Post-mating response Sex peptide receptor
Accessory gland proteins
Central nervous system
G protein-coupled receptor
Sex peptide receptor
The authors thank L. Vanden Bosch and J. Van Duppen for technical support, B. Breugelmans and V. van Hoef for supplying Bombyx and Tribolium cDNA, and M. Parmentier (University of Brussels, Belgium) and M. Detheux (Euroscreen S.A., Belgium) for providing WTA11 cells. The authors gratefully acknowledge the Interuniversity Attraction Poles program (Belgian Science Policy Grant P6/14), the Research Foundation of Flanders (FWO-Flanders), the K.U. Leuven Research Foundation (GOA 2005/06) and the USDA/DOD DWFP Initiative (#0500-32000-001-01R) (R.J.N). B.V.H. was supported by the IWT and J.P. obtained a postdoctoral research fellowship from FWO.