Fwmale oni x human male4/16/2023 b Schematic of spermatheca (red square in a) displaying the spermatheca secretory cells (SSC) radially organized around a lumen (L) where sperm (S) is stored. The female-RT is composed of ovaries (Ov), oviduct (Od), seminal receptacle (SR) and a pair of spermathecae (Spt), where sperm is stored, a pair of female accessory glands (femAG), and a uterus (Ut). Whether EVs are used by the SSC to modulate and coordinate female-RT activity to achieve high fertility, and what roles the male plays in such SSC-female-RT communication, is unknown.Ī Schematic of the female reproductive tract (female-RT adapted from Avila, F.W. In Drosophila, the male accessorygland secretory cells produce and secrete EVs which are transferred to the female during mating and inhibit her re-mating behavior 16. Given that EVs shuttle lipids, proteins, RNA, DNA, metabolites and other components, they can change the fate of recipient cells 15. EVs can emerge from the plasma membrane (microvesicles) or be derived from endosomal compartments and formed within multivesicular bodies (MVBs) (exosomes). EVs, a heterogeneous family of cell-derived vesicles, are released by most cell types and can elicit a phenotypic response in the secreting cell itself, or in neighboring and/or distant target cells. One possible mechanism by which the SSC regulate processes in other organs is via secretion of soluble factors and/or extracellular vesicles (EVs) into the reproductive tract environment 4. It is unclear how the SSC regulate these activities, but their effect on the female reproductive system is pronounced, as any modification in their function leads to a reduction in fertility. Furthermore, ablation of the SSC after female eclosion showed that SSC function is required for sperm to reach the spermatheca and retain motility while in storage, and for proper egg-laying 14. The transit of eggs through the female-RT requires Hr39 expression and non-canonical secretions 13. In addition, sperm storage in the spermatheca requires the expression of Hormone receptor-like in 39 ( Hr39, a nuclear hormone receptor and a master regulator of gland development) and canonical secretions from both glands. Simultaneous disruption of spermatheca and femAG development results in female sterility 12. In Drosophila melanogaster, formation of the female-RT environment is partially driven by spermathecal secretory cells (SSC), a layer of cuboidal secretory glandular cells that surrounds the spermatheca capsule where sperm is stored, and by the female accessory glands (femAG) 6, 10, 11 (Fig. The manner in which different combinations of input modalities and output networks lead to high fertility remains largely unresolved. In response to these cues, and together with the paternal contributions, the female reproductive tract (female-RT) coordinates the formation of an environment promoting gamete production, transport, maintenance and union, leading to healthy offspring 4, 5, 6, 7, 8, 9. Among these cues are signals transferred with sperm to the female in the seminal fluid, during copulation 1, 2, 3. In many species, including insects, male-female communication involves a complex combination of cues at multiple modalities that affect female physiology by manipulating female control of reproduction. Interactions between male and female, from pre-mating through post-mating, shift female physiology to accommodate high fertility. Thus, mating regulates secretory/endocytic pathways required for trafficking of vesicles to SSC-female-RT target sites, which modulate and coordinate reproductive tract activity to achieve high fertility. Moreover, sperm and male accessory gland proteins are essential for such mating-mediated SSC activity. The SSC release a heterogeneous population of extracellular vesicles (EVs) which is involved in initiating and managing the increase in egg-laying, and possibly sperm storage. Here we show that mating activates the secretory machinery of the SSC. It is unclear, however, how the SSC regulate the system’s activity. The SSC are a layer of cuboidal secretory glandular cells surrounding the spermatheca capsule where sperm is stored. In Drosophila, this modulation is partially driven by spermathecal secretory cells (SSC). The female reproductive tract (female-RT) must decipher the repertoire of molecular cues received from the male during copulation in order to activate and coordinate tract functionality necessary for high fertility.
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