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 BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions

2019 ◽  
Vol 116 (49) ◽  
pp. 24719-24728 ◽  
Author(s):  
Ben R. Hopkins ◽  
Irem Sepil ◽  
Sarah Bonham ◽  
Thomas Miller ◽  
Philip D. Charles ◽  
...  
Keyword(s):  
Seminal Fluid ◽  
Cell Types ◽  
Bmp Signaling ◽  
Secretory Cells ◽  
Normal Female ◽  
Seminal Fluid Proteins ◽  
Accessory Glands ◽  
Offspring Production ◽  
Morphogenetic Protein ◽  
And Function

Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of ∼1,000 fertility-enhancing “main cells” and ∼40 more functionally cryptic “secondary cells.” Inhibition of bone morphogenetic protein (BMP) signaling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female postmating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary-cell secretions might therefore make highly specific contributions to the seminal proteome and ejaculate function; alternatively, they might regulate more global—but hitherto undiscovered—SFP functions and proteome composition. Here, we present data that support the latter model. We show that in addition to previously reported phenotypes, secondary-cell-specific BMP signaling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal changes to the seminal proteome that surprisingly encompass alterations to main-cell–derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell types, suggesting that modification to the cellular make-up of seminal-fluid-producing tissues is an important factor in ejaculate evolution.

scholarly journals BMP-signalling inhibition in Drosophila secondary cells remodels the seminal proteome, and self and rival ejaculate functions

2019 ◽  
Author(s):  
Ben R. Hopkins ◽  
Irem Sepil ◽  
Sarah Bonham ◽  
Thomas Miller ◽  
Philip D. Charles ◽  
...  
Keyword(s):  
Seminal Fluid ◽  
Cell Types ◽  
Secretory Cells ◽  
Normal Female ◽  
Seminal Fluid Proteins ◽  
Accessory Glands ◽  
Offspring Production ◽  
Use Efficiency ◽  
Bmp Signalling ◽  
And Function

ABSTRACTSeminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of ∼1000 fertility-enhancing ‘main cells’ and ∼40, more functionally cryptic, ‘secondary cells’. Inhibition of BMP-signalling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female post-mating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary cell secretions might therefore make a highly specific contribution to the seminal proteome and ejaculate function; alternatively, they might regulate more global – but hitherto-undiscovered – SFP functions and proteome composition. Here, we present data that supports the latter model. We show that in addition to previously reported phenotypes, secondary cell-specific BMP-signalling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a novel constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal a mix of specific and widespread changes to the seminal proteome that surprisingly encompass alterations to main cell-derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell-types suggesting that modification to the cellular make-up of seminal fluid-producing tissues is an important factor in ejaculate evolution.

Dual role of the Pax genepairedin accessory gland development ofDrosophila

Development ◽  
2002 ◽  
Vol 129 (2) ◽  
pp. 339-346 ◽  
Author(s):  
Lei Xue ◽  
Markus Noll
Keyword(s):  
Male Fertility ◽  
Cell Types ◽  
Accessory Gland ◽  
Dual Role ◽  
Secretory Cells ◽  
Adult Males ◽  
Mating Activity ◽  
Promote Cell Proliferation ◽  
Accessory Glands ◽  
Late Function

The Drosophila Pax gene paired encodes a transcription factor that is required for the activation of segment-polarity genes and proper segmentation of the larval cuticle, postembryonic viability and male fertility. We show that paired executes a dual role in the development of male accessory glands, the organ homologous to the human prostate. An early function is necessary to promote cell proliferation, whereas a late function, which regulates the expression of accessory gland products such as the sex peptide and Acp26Aa protein, is essential for maturation and differentiation of accessory glands. The late function exhibits in main and secondary secretory cells of accessory glands dynamic patterns of Paired expression that depend in both cell types on the mating activity of adult males, possibly because Paired expression is regulated by negative feedback. The early Paired function depends on domains or motifs in its C-terminal moiety and the late function on the DNA-binding specificity of its N-terminal paired-domain and/or homeodomain. Both Paired functions are absolutely required for male fertility, and both depend on an enhancer located within 0.8 kb of the downstream region of paired.

scholarly journals FACS-based isolation and RNA extraction of Secondary Cells from the Drosophila male Accessory Gland

2019 ◽  
Author(s):  
Clément Immarigeon ◽  
François Karch ◽  
Robert K. Maeda
Keyword(s):  
Cell Population ◽  
Seminal Fluid ◽  
Rna Extraction ◽  
Cell Types ◽  
Accessory Gland ◽  
Specific Cell ◽  
Male Accessory Gland ◽  
Accessory Gland Proteins ◽  
Accessory Glands ◽  
Study Gene Expression

ABSTRACTTo appreciate the function of an organ, it is often critical to understand the role of rare cell populations. Unfortunately, this rarity often makes it difficult to obtain material for study. This is the case for the Drosophila male accessory gland, the functional homolog of mammalian prostate and seminal vesicle. In Drosophila, this gland is made up of two morphologically distinct cell types: the polygonally-shaped main cells, which compose 96% of the organ, and the larger, vacuole-containing secondary cells (SCs), which represent the remaining 4% of cells (~40 cells per lobe). Both cell types are known to produce accessory gland proteins (Acps), which are important components of the seminal fluid and are responsible for triggering multiple physiological and behavioral processes in females, collectively called the post-mating response (PMR). While a few genes are known to be specific to the SCs, the relative rarity of SCs has hindered the study of their whole transcriptome. Here, a method allowing for the isolation of SCs is presented, enabling the extraction and sequencing of RNAs from this rare cell population. The protocol consists of dissection, protease digestion and mechanical dissociation of the glands to obtain individual cells. Then, the cells are sorted by FACS, and living GFP-expressing SC singulets are isolated for RNA extraction. This procedure is able to provide SC-specific RNAs from ~40 males per condition in the course of one day. Given the speed and low number of flies required, this method enables the use of downstream RT-qPCR and/or RNA sequencing to the study gene expression in the SCs from different genetic backgrounds, ages, mating statuses or environmental conditions.SUMMARYHere, we describe the dissociation and sorting of a specific cell population from the Drosophila male accessory glands (Secondary cells), followed by RNA extraction for sequencing and RT-qPCR. The dissociation consists of dissection, proteases digestion and mechanical dispersion, followed by FACS purification of GFP-expressing cells.

Reproductive behaviour and physiology of Tenebrio molitor (Coleoptera: Tenebrionidae). III. Histogenetic changes in the internal genitalia, mesenteron, and cuticle during sexual maturation

1976 ◽  
Vol 54 (6) ◽  
pp. 990-1002 ◽  
Author(s):  
G. H. Gerber
Keyword(s):  
Sexual Maturation ◽  
Adult Life ◽  
Tenebrio Molitor ◽  
Reproductive Behaviour ◽  
Accessory Gland ◽  
Peritrophic Membrane ◽  
Secretory Cells ◽  
Accessory Glands ◽  
Internal Genitalia ◽  
Day By Day

The histogenic changes in the internal genitalia and mesenteron and the hardening and darkening of the cuticle during the first days of adult life in Tenebrio molitor L. are described. At emergence, the testes contain mature spermatozoa and the ovaries possess small oocytes. During the first 3 days, the shape, size, appearance, and staining characteristics of the secretory cells of the lateral oviducts, female accessory gland, tube accessory glands, bean-shaped accessory glands, and glandular region of the vasa deferentia change. Similar changes were not seen in the seminal vesicles and spermatheca. All of the secondary sex glands are filled with secretion by day 4. In the midgut, changes occur in the size, shape, and appearance of the epithelial cells by the 3rd day, and a peritrophic membrane is secreted during days 2 and 3. Most adults do not begin to feed until after the 3rd day. By day 3, the hardening and darkening of the cuticle are completed. All of these changes clearly are associated with adult maturation, especially sexual maturation, and most or all of the them must take place before the adults are able to copulate and oviposit.

scholarly journals Endocycles support tissue growth and regeneration of the adult Drosophila accessory gland

2019 ◽  
Author(s):  
Allison M. Box ◽  
Samuel Jaimian Church ◽  
David Hayes ◽  
Shyama Nandakumar ◽  
Russell S. Taichman ◽  
...  
Keyword(s):  
Cell Size ◽  
Seminal Fluid ◽  
Cell Types ◽  
Accessory Gland ◽  
Tissue Growth ◽  
Critical Function ◽  
Seminal Fluid Proteins ◽  
Functional Analog ◽  
Secretory Epithelial Cell ◽  
Adult Drosophila

AbstractThe Drosophila melanogaster accessory gland is a functional analog of the mammalian prostate made up of two secretory epithelial cell types, termed main and secondary cells. This tissue is responsible for making and secreting seminal fluid proteins and other molecules that contribute to successful reproduction. Here we show that similar to the mammalian prostate, this tissue grows with age. We find that the adult accessory gland grows in part via endocycles to increase DNA content and cell size, independent of mating status. The differentiated, bi-nucleated main cells remain poised to endocycle in the adult gland and upregulation of signals that promote endocycling and tissue growth are sufficient to trigger dramatic endocycling leading to increases in cell size and ploidy. The main cells of this tissue remain poised to enter the cell cycle and endocycling of main cells increases during recovery from severe tissue damage. Our data establish that the adult accessory gland is not quiescent, but instead uses endocycles to maintain the accessory gland’s critical function throughout the fruit fly’s lifespan.

scholarly journals Mating Induces Switch From Hormone-Dependent to – Independent Steroid Receptor-Mediated Growth in Drosophila Prostate-Like Cells

2019 ◽  
Author(s):  
Aaron Leiblich ◽  
Josephine E. E. U. Hellberg ◽  
Aashika Sekar ◽  
Carina Gandy ◽  
Siamak Redhai ◽  
...  
Keyword(s):  
Cancer Progression ◽  
Seminal Fluid ◽  
Sexual Experience ◽  
Adult Life ◽  
Accessory Gland ◽  
Accessory Glands ◽  
Morphogenetic Protein ◽  
A Cell ◽  
Cell Type Specific ◽  
Bmp Signalling

AbstractMale reproductive glands like the mammalian prostate and the paired Drosophila melanogaster accessory glands secrete seminal fluid components that enhance fecundity. In humans, the prostate grows throughout adult life, stimulated by environmentally regulated endocrine and local androgens. We previously showed that in each fly accessory gland, secondary cells (SCs) and their nuclei also grow in adults, a process enhanced by mating and controlled by bone morphogenetic protein (BMP) signalling. Here we demonstrate that BMP-mediated SC growth is dependent on the receptor for the developmental steroid, ecdysone, whose concentration reflects socio-sexual experience in adults. BMP signalling regulates ecdysone receptor (EcR) levels post-transcriptionally, partly via EcR’s N-terminus. Nuclear growth in virgin males is ecdysone-dependent. However, mating activates genome endoreplication to drive additional BMP-mediated nuclear growth via a cell type-specific form of hormone-independent EcR signalling. In virgin males with low ecdysone levels, this mechanism ensures resources are conserved. However, by switching to hormone-independence after mating, this control is overridden to hyper-activate growth of secretory secondary cells. Our data suggest parallels between this physiological, behaviour-induced switch and altered pathological signalling associated with prostate cancer progression.

Formation of spermatophore in ejaculatory duct of yellow mealworm beetle, Tenebrio molitor: SEM study

1992 ◽  
Vol 50 (1) ◽  
pp. 674-675
Author(s):  
Frantíšek Weyda ◽  
George M. Happ
Keyword(s):  
Seminal Fluid ◽  
Ejaculatory Duct ◽  
Tenebrio Molitor ◽  
High Viscosity ◽  
Secretory Cells ◽  
Main Role ◽  
Whole Process ◽  
Accessory Glands ◽  
Low Viscosity ◽  
Mealworm Beetle

Main role of the accessory glands of Tenebrio molitor male is to facilitate transfer of sperm to the females. They produce heterogeneous secretions. Two anatomically distinct glands are present. While the tubular accessory glands (TAG) are composed of the secretory cells of one type only, the bean-shaped accessory glands (BAG) consist of eight cellular types. Low viscosity secretion of the TAG mix with sperms forming seminal fluid while high viscosity secretions (spermatophorins) of the BAG are largely transformed into the insoluble wall and core of the spermatophore. The prespermatophoric mass is transferred to the ejaculatory duct (EJD) where solidify and forms the complex spermatophore. Immunocytochemical experiments with monoclonal antibodies based on the colloidal gold technique were used in order to understand exact composition of individual layers of the spermatophore. In the recent study we have used SEM to observe the whole process of the formation of spermatophore in the ejaculatory duct.

Single-nucleus transcriptomes reveal evolutionary and functional properties of cell types in the Drosophila accessory gland

Genetics ◽  
2021 ◽  
Author(s):  
Alex C Majane ◽  
Julie M Cridland ◽  
David J Begun
Keyword(s):  
Seminal Fluid ◽  
Ejaculatory Duct ◽  
Evolutionary Process ◽  
Cell Types ◽  
Accessory Gland ◽  
Male Reproduction ◽  
Seminal Fluid Proteins ◽  
Cell Diversity ◽  
Single Nucleus ◽  
First Time

Abstract Many traits responsible for male reproduction evolve quickly, including gene expression phenotypes in germline and somatic male reproductive tissues. Rapid male evolution in polyandrous species is thought to be driven by competition among males for fertilizations and conflicts between male and female fitness interests that manifest in post-copulatory phenotypes. In Drosophila, seminal fluid proteins secreted by three major cell types of the male accessory gland and ejaculatory duct are required for female sperm storage and use, and influence female post-copulatory traits. Recent work has shown that these cell types have overlapping but distinct effects on female post-copulatory biology, yet relatively little is known about their evolutionary properties. Here we use single-nucleus RNA-Seq of the accessory gland and ejaculatory duct from Drosophila melanogaster and two closely related species to comprehensively describe the cell diversity of these tissues and their transcriptome evolution for the first time. We find that seminal fluid transcripts are strongly partitioned across the major cell types, and expression of many other genes additionally define each cell type. We also report previously undocumented diversity in main cells. Transcriptome divergence was found to be heterogeneous across cell types and lineages, revealing a complex evolutionary process. Furthermore, protein adaptation varied across cell types, with potential consequences for our understanding of selection on male post-copulatory traits.

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.

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