Control of oocyte maturation in sexually mature Drosophila females.
In many sexually mature insects egg production and oviposition are tightly coupled to copulation. Sex-Peptide is a 36-amino-acid peptide synthesized in the accessory glands of Drosophila melanogaster males and transferred to the female during copulation. Sex-Peptide stimulates vitellogenic oocyte progression through a putative control point at about stage 9 of oogenesis. Here we show that application of the juvenile hormone analogue methoprene mimics the Sex-Peptide-mediated stimulation of vitellogenic oocyte progression in sexually mature virgin females. Apoptosis is induced by 20-hydroxyecdysone in nurse cells of stage 9 egg chambers at physiological concentrations (10(-7) M). 20-Hydroxyecdysone thus acts as an antagonist of early vitellogenic oocyte development. Simultaneous application of juvenile hormone analogue, however, protects early vitellogenic oocytes from 20-hydroxyecdysone-induced resorption. These results suggest that the balance of these hormones in the hemolymph regulates whether oocytes will progress through the control point at stage 9 or undergo apoptosis. These data are further supported by a molecular analysis of the regulation of yolk protein synthesis and uptake into the ovary by the two hormones. We conclude that juvenile hormone is a downstream component in the Sex-Peptide response cascade and acts by stimulating vitellogenic oocyte progression and inhibiting apoptosis. Since juvenile hormone analogue does not elicit increased oviposition and reduced receptivity, Sex-Peptide must have an additional, separate effect on these two postmating responses.
Soller
M
M
Zoologisches Institut, Universität Zürich-Irchel, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.
Bownes
M
M
Kubli
E
E
D000818:Animals; D017209:Apoptosis / Q000187:drug effects; D003307:Copulation; D004305:Dose-Response Relationship, Drug; D029721:Drosophila Proteins; D004331:Drosophila melanogaster / Q000166:cytology*; D004441:Ecdysterone / Q000494:pharmacology*; D004527:Egg Proteins / Q000096:biosynthesis / Q000235:genetics; D005260:Female; D006458:Hemolymph / Q000737:chemistry; D036341:Intercellular Signaling Peptides and Proteins; D008726:Methoprene / Q000494:pharmacology*; D008954:Models, Biological; D018716:Molecular Mimicry; D010058:Oviposition / Q000187:drug effects; D010455:Peptides / Q000494:pharmacology*; D012333:RNA, Messenger / Q000032:analysis; D015398:Signal Transduction; D014818:Vitellogenesis / Q000187:drug effects*
D029721:Drosophila Proteins; D004441:Ecdysterone; D004527:Egg Proteins; D036341:Intercellular Signaling Peptides and Proteins; D008726:Methoprene; D010455:Peptides; D012333:RNA, Messenger; C489177:Acp36DE protein, Drosophila; C056736:SP protein, Drosophila