scholarly journals Drosophila Sex Peptide controls the assembly of lipid microcarriers in seminal fluid

2021 ◽  
Vol 118 (5) ◽  
pp. e2019622118
Author(s):  
S. Mark Wainwright ◽  
Ben R. Hopkins ◽  
Cláudia C. Mendes ◽  
Aashika Sekar ◽  
Benjamin Kroeger ◽  
...  
Keyword(s):  
Seminal Fluid ◽  
Fruit Fly ◽  
Male Reproductive Success ◽  
Mutant Proteins ◽  
Macromolecular Assemblies ◽  
Sex Peptide ◽  
Accessory Glands ◽  
Storage Organs ◽  
Paired Male ◽  
Male Specific

Seminal fluid plays an essential role in promoting male reproductive success and modulating female physiology and behavior. In the fruit fly, Drosophila melanogaster, Sex Peptide (SP) is the best-characterized protein mediator of these effects. It is secreted from the paired male accessory glands (AGs), which, like the mammalian prostate and seminal vesicles, generate most of the seminal fluid contents. After mating, SP binds to spermatozoa and is retained in the female sperm storage organs. It is gradually released by proteolytic cleavage and induces several long-term postmating responses, including increased ovulation, elevated feeding, and reduced receptivity to remating, primarily signaling through the SP receptor (SPR). Here, we demonstrate a previously unsuspected SPR-independent function for SP. We show that, in the AG lumen, SP and secreted proteins with membrane-binding anchors are carried on abundant, large neutral lipid-containing microcarriers, also found in other SP-expressing Drosophila species. These microcarriers are transferred to females during mating where they rapidly disassemble. Remarkably, SP is a key microcarrier assembly and disassembly factor. Its absence leads to major changes in the seminal proteome transferred to females upon mating. Males expressing nonfunctional SP mutant proteins that affect SP’s binding to and release from sperm in females also do not produce normal microcarriers, suggesting that this male-specific defect contributes to the resulting widespread abnormalities in ejaculate function. Our data therefore reveal a role for SP in formation of seminal macromolecular assemblies, which may explain the presence of SP in Drosophila species that lack the signaling functions seen in D. melanogaster.

scholarly journals Drosophila Sex Peptide Controls the Assembly of Lipid Microcarriers in Seminal Fluid

2020 ◽  
Author(s):  
S. Mark Wainwright ◽  
Cláudia C. Mendes ◽  
Aashika Sekar ◽  
Benjamin Kroeger ◽  
Josephine E.E.U. Hellberg ◽  
...  
Keyword(s):  
Reproductive Success ◽  
Neutral Lipid ◽  
Seminal Fluid ◽  
Critical Role ◽  
Fruit Fly ◽  
Male Reproductive Success ◽  
Sex Peptide ◽  
Accessory Glands ◽  
Assembly Factor ◽  
Female Physiology

AbstractSeminal fluid plays an essential role in promoting male reproductive success and modulating female physiology and behaviour. In the fruit fly, Drosophila melanogaster, Sex Peptide (SP) is the best-characterised protein mediator of these effects. It is secreted from the paired male accessory glands (AGs), which, like the mammalian prostate and seminal vesicles, generate most of the seminal fluid contents. After mating, SP binds to spermatozoa and is retained in the female sperm storage organs. It is gradually released by proteolytic cleavage and induces several long-term post-mating responses including ovulation, elevated feeding and reduced receptivity to remating, primarily signalling through the SP receptor (SPR). Here, we demonstrate a previously unsuspected SPR-independent function for SP. We show that, in the AG lumen, SP and secreted proteins with membrane-binding anchors are carried on abundant, large neutral lipid-containing microcarriers, also found in other SP-expressing Drosophila species. These microcarriers are transferred to females during mating, where they rapidly disassemble. Remarkably, SP is a key assembly factor for microcarriers and is also required for the female disassembly process to occur normally. Males expressing non-functional SP mutant proteins that affect SP’s binding to and release from sperm in females also do not produce normal microcarriers, suggesting that this male-specific defect contributes to the resulting widespread defects in ejaculate function. Our data therefore reveal a novel role for SP in formation of seminal macromolecular assemblies, which may explain the presence of SP in Drosophila species, which lack the signalling functions seen in D. melanogaster.Significance StatementSeminal fluid plays a critical role in reprogramming female physiology and behaviour to promote male reproductive success. We show in the fruit fly that specific seminal proteins, including the archetypal ‘female-reprogramming’ molecule Sex Peptide, are stored in male seminal secretions in association with large neutral lipid-containing microcarriers, which rapidly disperse in females. Related structures are also observed in other Sex Peptide-expressing Drosophila species. Males lacking Sex Peptide have structurally defective microcarriers, leading to abnormal cargo loading and transfer to females. Our data reveal that this key signalling molecule in Drosophila seminal fluid is also a microcarrier assembly factor that controls transfer of other seminal factors, and that this may be a more evolutionarily ancient role of this protein.

scholarly journals Regulation of Mating-Induced Increase in Female Germline Stem Cells in the Fruit Fly Drosophila melanogaster

2021 ◽  
Vol 12 ◽  
Author(s):  
Ryo Hoshino ◽  
Ryusuke Niwa
Keyword(s):  
Stem Cells ◽  
Drosophila Melanogaster ◽  
Energy Demand ◽  
Seminal Fluid ◽  
Fruit Fly ◽  
Egg Laying ◽  
Germline Stem Cells ◽  
Humoral Factors ◽  
Mating Response ◽  
Sex Peptide

In many insect species, mating stimuli can lead to changes in various behavioral and physiological responses, including feeding, mating refusal, egg-laying behavior, energy demand, and organ remodeling, which are collectively known as the post-mating response. Recently, an increase in germline stem cells (GSCs) has been identified as a new post-mating response in both males and females of the fruit fly, Drosophila melanogaster. We have extensively studied mating-induced increase in female GSCs of D. melanogaster at the molecular, cellular, and systemic levels. After mating, the male seminal fluid peptide [e.g. sex peptide (SP)] is transferred to the female uterus. This is followed by binding to the sex peptide receptor (SPR), which evokes post-mating responses, including increase in number of female GSCs. Downstream of SP-SPR signaling, the following three hormones and neurotransmitters have been found to act on female GSC niche cells to regulate mating-induced increase in female GSCs: (1) neuropeptide F, a peptide hormone produced in enteroendocrine cells; (2) octopamine, a monoaminergic neurotransmitter synthesized in ovary-projecting neurons; and (3) ecdysone, a steroid hormone produced in ovarian follicular cells. These humoral factors are secreted from each organ and are received by ovarian somatic cells and regulate the strength of niche signaling in female GSCs. This review provides an overview of the latest findings on the inter-organ relationship to regulate mating-induced female GSC increase in D. melanogaster as a model. We also discuss the remaining issues that should be addressed in the future.

scholarly journals Sexual conflict over remating interval is modulated by the sex peptide pathway

2017 ◽  
Vol 284 (1850) ◽  
pp. 20162394 ◽  
Author(s):  
Damian T. Smith ◽  
Naomi V. E. Clarke ◽  
James M. Boone ◽  
Claudia Fricke ◽  
Tracey Chapman
Keyword(s):  
Sexual Conflict ◽  
Fruit Fly ◽  
Window Of Opportunity ◽  
Reproductive Systems ◽  
Peptide Receptor ◽  
Conflict And Cooperation ◽  
Sex Peptide ◽  
Selective Forces ◽  
Males And Females ◽  
Male Specific

Sexual conflict, in which the evolutionary interests of males and females diverge, shapes the evolution of reproductive systems across diverse taxa. Here, we used the fruit fly to study sexual conflict in natural, three-way interactions comprising a female, her current and previous mates. We manipulated the potential for sexual conflict by using sex peptide receptor ( SPR ) null females and by varying remating from 3 to 48 h, a period during which natural rematings frequently occur. SPR -lacking females do not respond to sex peptide (SP) transferred during mating and maintain virgin levels of high receptivity and low fecundity. In the absence of SPR, there was a convergence of fitness interests, with all individuals gaining highest productivity at 5 h remating. This suggests that the expression of sexual conflict was reduced. We observed an unexpected second male-specific advantage to early remating, resulting from an increase in the efficiency of second male sperm use. This early window of opportunity for exploitation by second males depended on the presence of SPR . The results suggest that the SP pathway can modulate the expression of sexual conflict in this system, and show how variation in the selective forces that shape conflict and cooperation can be maintained.

scholarly journals Morphological and Developmental Traits of the Binucleation of Male Accessory Gland Cells in the Benthic Water Bug, Aphelocheirus vittatus (Hemiptera: Aphelochiridae)

2020 ◽  
Vol 20 (4) ◽  
Author(s):  
Koji Takeda ◽  
Jun Yamauchi ◽  
Takashi Adachi-Yamada
Keyword(s):  
Epithelial Cells ◽  
Cell Fusion ◽  
Seminal Fluid ◽  
Physiological Role ◽  
Reproductive Organs ◽  
Accessory Gland ◽  
Male Reproductive Success ◽  
Reproductive Behaviors ◽  
Accessory Glands ◽  
Close Relationship

Abstract The male accessory glands (MAGs) in insects are pair(s) of internal reproductive organs that produce and secrete the plasma component of seminal fluid. In various insects, MAG size is important for male reproductive success because the fluid provides physiologically active substances and/or nutrients to females to control sperm as well as female reproductive behaviors. Although the MAG epithelial cells in most insect species are standard mononucleate cells, those in some insect taxa are binucleate due to incomplete cytokinesis (e.g., Drosophila [Fallén] [Diptera: Drosophilidae]) or cell fusion (e.g., Cimex [Linnaeus] [Hemiptera: Cimicidae]). In the case of Drosophila, the apicobasal position of the two nuclei relative to the epithelial plane changes from vertical to horizontal after nutrient intake, which allows the volume of the MAG cavity to expand effectively. On the other hand, in the case of Cimex, the positions of the two nuclei do not change apicobasally in response to feeding, but their position relative to the proximodistal axis varies depending on the tubular/spherical organ morphology. Here, we report that the MAG of the benthic water bug Aphelocheirus vittatus (Matsumura) (Hemiptera: Aphelochiridae) shows binucleation in all epithelial cells. Despite the phylogenetically close relationship between Aphelocheirus and Cimex, the MAG cells in Aphelocheirus showed a Drosophila-like apicobasal change in the position of the two nuclei in response to feeding. Furthermore, the cytological processes during binucleation are more similar to those in Drosophila (incomplete cytokinesis) than to those in Cimex (cell fusion). These results indicate that the physiological role and mechanism of binucleation in MAG cells changed during the evolution of Hemiptera.

scholarly journals Identification of a micropeptide and multiple secondary cell genes that modulate Drosophila male reproductive success

2021 ◽  
Vol 118 (15) ◽  
pp. e2001897118
Author(s):  
Clément Immarigeon ◽  
Yohan Frei ◽  
Sofie Y. N. Delbare ◽  
Dragan Gligorov ◽  
Pedro Machado Almeida ◽  
...  
Keyword(s):  
Seminal Fluid ◽  
Accessory Gland ◽  
Micro Rna ◽  
Open Reading Frames ◽  
Male Reproductive Success ◽  
Loss Of Function ◽  
Cell Type ◽  
Small Peptides ◽  
Male Specific ◽  
Small Orfs

Even in well-characterized genomes, many transcripts are considered noncoding RNAs (ncRNAs) simply due to the absence of large open reading frames (ORFs). However, it is now becoming clear that many small ORFs (smORFs) produce peptides with important biological functions. In the process of characterizing the ribosome-bound transcriptome of an important cell type of the seminal fluid-producing accessory gland of Drosophila melanogaster, we detected an RNA, previously thought to be noncoding, called male-specific abdominal (msa). Notably, msa is nested in the HOX gene cluster of the Bithorax complex and is known to contain a micro-RNA within one of its introns. We find that this RNA encodes a “micropeptide” (9 or 20 amino acids, MSAmiP) that is expressed exclusively in the secondary cells of the male accessory gland, where it seems to accumulate in nuclei. Importantly, loss of function of this micropeptide causes defects in sperm competition. In addition to bringing insights into the biology of a rare cell type, this work underlines the importance of small peptides, a class of molecules that is now emerging as important actors in complex biological processes.

The Drosophila melanogaster X-Linked mfs(1)6E Locus Is Required for Production of Normal Seminal Fluid by the Male Accessory Glands

2001 ◽  
Vol 267 (1) ◽  
pp. 1-12 ◽  
Author(s):  
Pedro P. López ◽  
Juán F. Santarén ◽  
M.Fernanda Ruiz ◽  
Pedro Esponda ◽  
Lucas Sánchez
Keyword(s):  
Drosophila Melanogaster ◽  
Seminal Fluid ◽  
Male Accessory Glands ◽  
Accessory Glands

scholarly journals Rab-mediated trafficking in the secondary cells of Drosophila male accessory glands and its role in fecundity

2018 ◽  
Author(s):  
E. Prince ◽  
M. Brankatschk ◽  
B. Kroeger ◽  
D. Gligorov ◽  
C. Wilson ◽  
...  
Keyword(s):  
Mating Behavior ◽  
Seminal Fluid ◽  
Cell Types ◽  
Accessory Gland ◽  
Molecular Organization ◽  
Secretory Cells ◽  
Rab Proteins ◽  
Intracellular Membrane ◽  
Accessory Glands ◽  
Intracellular Membrane Transport

AbstractIt is known that the male seminal fluid contains factors that affect female post-mating behavior and physiology. In Drosophila, most of these factors are secreted by the two epithelial cell types that make up the male accessory gland: the main and secondary cells. Although secondary cells represent only 4% of the cells of the accessory gland, their contribution to the male seminal fluid is essential for sustaining the female post-mating response. To better understand the function of the secondary cells, here we investigate their molecular organization, particularly with respect to the intracellular membrane transport machinery. We determined that large vacuole-like structures found in the secondary cells are trafficking hubs labeled by Rab6, 7, 11 and 19. Furthermore, these cell-specific organelles are essential for the long-term post-mating behavior of females and that their formation is directly dependent upon Rab6. Our discovery adds to our understanding of Rab proteins function in secretory cells. We have created an online, open-access imaging resource as a valuable tool for the intracellular membrane and protein traffic community.

scholarly journals Targeting the autosomal Ceratitis capitata transformer gene using Cas9 or dCas9 to masculinize XX individuals without inducing mutations

BMC Genetics ◽  
2020 ◽  
Vol 21 (S2) ◽  
Author(s):  
Pasquale Primo ◽  
Angela Meccariello ◽  
Maria Grazia Inghilterra ◽  
Andrea Gravina ◽  
Giuseppe Del Corsano ◽  
...  
Keyword(s):  
Sex Determination ◽  
Ceratitis Capitata ◽  
Mutagenic Activity ◽  
Fruit Fly ◽  
Agricultural Pests ◽  
Guide Rna ◽  
Xx Males ◽  
Biallelic Mutations ◽  
Female Specific ◽  
Male Specific

Abstract Background Females of the Mediterranean fruit fly Ceratitis capitata (Medfly) are major agricultural pests, as they lay eggs into the fruit crops of hundreds of plant species. In Medfly, female sex determination is based on the activation of Cctransformer (Cctra). A maternal contribution of Cctra is required to activate Cctra itself in the XX embryos and to start and epigenetically maintain a Cctra positive feedback loop, by female-specific alternative splicing, leading to female development. In XY embryos, the male determining Maleness-on-the-Y gene (MoY) blocks this activation and Cctra produces male-specific transcripts encoding truncated CcTRA isoforms and male differentiation occurs. Results With the aim of inducing frameshift mutations in the first coding exon to disrupt both female-specific and shorter male-specific CcTRA open reading frames (ORF), we injected Cas9 ribonucleoproteins (Cas9 and single guide RNA, sgRNA) in embryos. As this approach leads to mostly monoallelic mutations, masculinization was expected only in G1 XX individuals carrying biallelic mutations, following crosses of G0 injected individuals. Surprisingly, these injections into XX-only embryos led to G0 adults that included not only XX females but also 50% of reverted fertile XX males. The G0 XX males expressed male-specific Cctra transcripts, suggesting full masculinization. Interestingly, out of six G0 XX males, four displayed the Cctra wild type sequence. This finding suggests that masculinization by Cas9-sgRNA injections was independent from its mutagenic activity. In line with this observation, embryonic targeting of Cctra in XX embryos by a dead Cas9 (enzymatically inactive, dCas9) also favoured a male-specific splicing of Cctra, in both embryos and adults. Conclusions Our data suggest that the establishment of Cctra female-specific autoregulation during the early embryogenesis has been repressed in XX embryos by the transient binding of the Cas9-sgRNA on the first exon of the Cctra gene. This hypothesis is supported by the observation that the shift of Cctra splicing from female to male mode is induced also by dCas9. Collectively, the present findings corroborate the idea that a transient embryonic inactivation of Cctra is sufficient for male sex determination.

tert-Pentyl 4 (and 5)-chloro-trans-2-methylcyclohexanecarboxylate, a Highly Effective and Persistent Male Specific Attractant for the Mediterranean Fruit Fly (Diptera: Tephritidae)2

1999 ◽  
Vol 34 (1) ◽  
pp. 119-125
Author(s):  
Albert B. DeMilo ◽  
Roy T. Cunningham ◽  
Terrence P. McGovern
Keyword(s):  
Natural Population ◽  
Dose Response ◽  
Ceratitis Capitata ◽  
Field Tests ◽  
Fruit Fly ◽  
Mediterranean Fruit Fly ◽  
Response Data ◽  
Isomer Distribution ◽  
Male Specific ◽  
Dental Roll

The attraction of male Ceratitis capitata (Wiedemann) to tert-pentyl 4(and 5)-chloro-trans-2-methylcyclohexanecarboxylate (or pentamedlure) was compared to its attraction to trimedlure to establish the suitability of pentamedlure as a possible alternate for trimedlure in applications that use a cotton dental-roll wick dispenser. Results from field tests with released sterile C. capitata showed that pentamedlure, applied to cotton dental roll wicks, was not only comparable to trimedlure in attractiveness but was more persistent. Batch to batch variations in isomer distribution of pentamedlure appeared to have little effect on attraction. Dose-response data showed that pentamedlure, applied at 0.02 and 0.16 ml/wick, initially caught more flies than trimedlure at comparable doses. Moreover, initial catches for pentamedlure for most dosages tested exceeded, but not significantly, initial catches for trimedlure despite a much higher load (2 ml/wick). Trimedlure initial catches within a natural population of wild C. capitata were significantly higher than pentamedlure catches at a comparable dosage (0.2 ml lure/wick). However, pentamedlure-treated wicks were 2 to 3 times more persistent than wicks treated with trimedlure.

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