RESUMO
Animal embryos are provided by their mothers with a diverse nutrient supply that is crucial for development. In Drosophila, the three most abundant nutrients (triglycerides, proteins and glycogen) are sequestered in distinct storage structures: lipid droplets (LDs), yolk vesicles (YVs) and glycogen granules (GGs). Using transmission electron microscopy as well as live and fixed sample fluorescence imaging, we find that all three storage structures are dispersed throughout the egg but are then spatially allocated to distinct tissues by gastrulation: LDs largely to the peripheral epithelium, YVs and GGs to the central yolk cell. To confound the embryo's ability to sort its nutrients, we employ Jabba and mauve mutants to generate LD-GG and LD-YV compound structures. In these mutants, LDs are mis-sorted to the yolk cell and their turnover is delayed. Our observations demonstrate dramatic spatial nutrient sorting in early embryos and provide the first evidence for its functional importance.
Assuntos
Proteínas de Drosophila , Drosophila , Animais , Drosophila/metabolismo , Proteínas de Drosophila/metabolismo , Transporte Proteico , Nutrientes , Gotículas Lipídicas/metabolismo , Glicogênio/metabolismo , Metabolismo dos Lipídeos , Proteínas de Transporte/metabolismoRESUMO
Lipid droplets (LDs), crucial regulators of lipid metabolism, accumulate during oocyte development. However, their roles in fertility remain largely unknown. During Drosophila oogenesis, LD accumulation coincides with the actin remodeling necessary for follicle development. Loss of the LD-associated Adipose Triglyceride Lipase (ATGL) disrupts both actin bundle formation and cortical actin integrity, an unusual phenotype also seen when the prostaglandin (PG) synthase Pxt is missing. Dominant genetic interactions and PG treatment of follicles indicate that ATGL acts upstream of Pxt to regulate actin remodeling. Our data suggest that ATGL releases arachidonic acid (AA) from LDs to serve as the substrate for PG synthesis. Lipidomic analysis detects AA-containing triglycerides in ovaries, and these are increased when ATGL is lost. High levels of exogenous AA block follicle development; this is enhanced by impairing LD formation and suppressed by reducing ATGL. Together, these data support the model that AA stored in LD triglycerides is released by ATGL to drive the production of PGs, which promote the actin remodeling necessary for follicle development. We speculate that this pathway is conserved across organisms to regulate oocyte development and promote fertility.
Assuntos
Proteínas de Drosophila , Prostaglandinas , Animais , Gotículas Lipídicas , Actinas , Adipogenia , Drosophila , Lipase , Peroxidases , Proteínas de Drosophila/genéticaRESUMO
Because both dearth and overabundance of histones result in cellular defects, histone synthesis and demand are typically tightly coupled. In Drosophila embryos, histones H2B, H2A and H2Av accumulate on lipid droplets (LDs), which are cytoplasmic fat storage organelles. Without LD binding, maternally provided H2B, H2A and H2Av are absent; however, how LDs ensure histone storage is unclear. Using quantitative imaging, we uncover when during oogenesis these histones accumulate, and which step of accumulation is LD dependent. LDs originate in nurse cells (NCs) and are transported to the oocyte. Although H2Av accumulates on LDs in NCs, the majority of the final H2Av pool is synthesized in oocytes. LDs promote intercellular transport of the histone anchor Jabba and thus its presence in the ooplasm. Ooplasmic Jabba then prevents H2Av degradation, safeguarding the H2Av stockpile. Our findings provide insight into the mechanism for establishing histone stores during Drosophila oogenesis and shed light on the function of LDs as protein-sequestration sites.
Assuntos
Histonas/metabolismo , Gotículas Lipídicas/metabolismo , Animais , Proteínas de Transporte/metabolismo , Drosophila/metabolismo , Proteínas de Drosophila/metabolismo , Feminino , Oócitos/metabolismo , Oogênese/fisiologiaRESUMO
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 Summary: How 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.
RESUMO
New work reveals differences in oogenic gene expression between parthenogenetic and sexually reproducing Drosophila mercatorum strains. Recapitulating those changes in D. melanogaster oocytes induced parthenogenesis in this normally sexually reproducing species, providing molecular insight into how these reproductive modes arise.