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Data of sperm-entry inability in Drosophila melanogaster ovarian follicles that are depleted of s36 chorionic protein.

ABSTRACT: This paper presents data associated with the research article entitled "Targeted downregulation of s36 protein unearths its cardinal role in chorion biogenesis and architecture during Drosophila melanogaster oogenesis" [1]. Drosophila chorion is produced by epithelial follicle cells and one of its functional serving role is egg fertilization through the micropyle, a specialized narrow channel at the anterior tip of the egg [2]. Sperm entry during fertilization is necessary for the egg to complete meiosis [3]. D. melanogaster flies being characterized by severe downregulation of the s36 chorionic protein, specifically in the follicle-cell compartment of their ovary, appear with impaired fly fertility (Velentzas et al., 2016) [1]. In an effort to further investigate whether the observed infertility in the s36-targeted flies derives from a fertilization failure, such as the inability of sperm to pass through egg?s micropyle, we mated females carrying s36-depleted ovaries with males expressing the GFP protein either in their sperm tails, or in both their sperm tails and sperm heads.

SUBMITTER: Velentzas AD

PROVIDER: S-EPMC5394213 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Data of sperm-entry inability in Drosophila melanogaster ovarian follicles that are depleted of s36 chorionic protein.

Velentzas Athanassios D AD Velentzas Panagiotis D PD Katarachia Stamatia S Mpakou Vassiliki E VE Papassideri Issidora S IS Stravopodis Dimitrios J DJ

Data in brief 20170408

This paper presents data associated with the research article entitled "Targeted downregulation of s36 protein unearths its cardinal role in chorion biogenesis and architecture during Drosophila melanogaster oogenesis" [1]. Drosophila chorion is produced by epithelial follicle cells and one of its functional serving role is egg fertilization through the micropyle, a specialized narrow channel at the anterior tip of the egg [2]. Sperm entry during fertilization is necessary for the ...[more]

PMID: 28443296

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Project description:New genes arise through a variety of evolutionary processes and provide raw material for adaptation in the face of both natural and sexual selection. De novo evolved genes emerge from previously non-protein-coding DNA sequences, and many such genes are expressed in male reproductive structures. In Drosophila melanogaster , several putative de novo genes have evolved essential roles in spermatogenesis, but whether such genes can also impact sperm function beyond the male has not been investigated. We identified a putative de novo gene, katherine johnson ( kj ), that is required for high levels of male fertility. Males that do not express kj produce and transfer sperm that are stored normally in females, but sperm from these males enter eggs with severely reduced efficiency. Using a tagged transgenic rescue construct, we observed that KJ protein localizes to the nuclear periphery in various stages of spermatogenesis, but is not detectable in mature sperm. These data suggest that kj exerts an effect on sperm development, the loss of which results in reduced fertilization ability. While previous bioinformatic analyses suggested the kj gene was restricted to the melanogaster group of Drosophila , we identified putative orthologs with conserved synteny, male-biased expression, and predicted protein features across the genus, as well as instances of gene loss in some lineages. Thus, kj potentially arose in the Drosophila common ancestor and subsequently evolved an essential role in D. melanogaster . Our results demonstrate a new aspect of male reproduction that has been shaped by new gene evolution and provide a molecular foothold for further investigating the mechanism of sperm entry into eggs in Drosophila .Article summaryHow fruit fly sperm enter eggs is poorly understood. Here, we identify a gene that potentially arose from non-protein-coding DNA and is required for efficient fertilization. Sperm from males lacking this gene's function cannot enter eggs. The gene appears to act during sperm production, rather than in mature sperm. This study illustrates how newly evolved genes can affect important aspects of reproduction and provides insights into sperm-egg interactions.

Project description:BackgroundMale-derived seminal fluid proteins (SFPs) that enter female fruitflies during mating induce a myriad of physiological and behavioral changes, optimizing fertility of the mating pair. Some post-mating changes in female Drosophila melanogaster persist for ~10-14 days. Their long-term persistence is because the seminal protein that induces these particular changes, the Sex Peptide (SP), is retained long term in females by binding to sperm, with gradual release of its active domain from sperm. Several other "long-term response SFPs" (LTR-SFPs) "prime" the binding of SP to sperm. Whether female factors play a role in this process is unknown, though it is important to study both sexes for a comprehensive physiological understanding of SFP/sperm interactions and for consideration in models of sexual conflict.ResultsWe report here that sperm in male ejaculates bind SP more weakly than sperm that have entered females. Moreover, we show that the amount of SP, and other SFPs, bound to sperm increases with time and transit of individual seminal proteins within the female reproductive tract (FRT). Thus, female contributions are needed for maximal and appropriate binding of SP, and other SFPs, to sperm. Towards understanding the source of female molecular contributions, we ablated spermathecal secretory cells (SSCs) and/or parovaria (female accessory glands), which contribute secretory proteins to the FRT. We found no dramatic change in the initial levels of SP bound to sperm stored in mated females with ablated or defective SSCs and/or parovaria, indicating that female molecules that facilitate the binding of SP to sperm are not uniquely derived from SSCs and parovaria. However, we observed higher levels of SP (and sperm) retention long term in females whose SSCs and parovaria had been ablated, indicating secretions from these female tissues are necessary for the gradual release of Sex Peptide's active region from stored sperm.ConclusionThis study reveals that the SP-sperm binding pathway is not entirely male-derived and that female contributions are needed to regulate the levels of SP associated with sperm stored in their storage sites.

Dataset Information

Data of sperm-entry inability in Drosophila melanogaster ovarian follicles that are depleted of s36 chorionic protein.

Publications

Data of sperm-entry inability in <i>Drosophila melanogaster</i> ovarian follicles that are depleted of s36 chorionic protein.

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