Germline stem cells play a pivotal role in gametogenesis; yet little is known about how they are formed, how they divide to self-renew, and how these processes are genetically controlled. Here we describe the self-renewing asymmetric division of germline stem cells in the Drosophila ovarian germline, as marked by the spectrosome, a cytoplasmic structure rich in membrane skeletal proteins. The ontogeny of the spectrosome marks the lineage of germline stem cells. We identified two new groups of mutations in which the divisional asymmetry is disrupted. The first, which we refer to as ovarette (ovt) mutations, was shown to correspond to a novel class of mutations in the pumilio locus. Since pumilio is known to posttranscriptionally repress the expression of target genes at earlier stages of germ cell development, our results suggest that a similar activity is needed to maintain germ line stem cells. We have also identified a second and novel gene, piwi, whose mutations abolish germline stem cell division.

A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary

Oogenesis in Drosophila takes place within germline cysts that support polarized transport through ring canals interconnecting their 15 nurse cells and single oocyte. Developing cystocytes are spanned by a large cytoplasmic structure known as the fusome that has been postulated to help form ring canals and determine the pattern of nurse cell-oocyte interconnections. We identified the adducin-like hts product and alpha-spectrin as molecular components of fusomes, discovered a related structure in germline stem cells and documented regular associations between fusomes and cystocyte centrosomes. hts mutations completely eliminated fusomes, causing abnormal cysts containing a reduced number of cells to form. Our results imply that Drosophila fusomes are required for ovarian cyst formation and suggest that membrane skeletal proteins regulate cystocyte divisions.

The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation

The Drosophila germline lineage depends on a complex microenvironment of extrinsic and intrinsic factors that regulate the self-renewing and asymmetric divisions of dedicated stem cells. Germline stem cells (GSCs) must express components of the Dpp cassette and the translational repressors Nanos and Pumilio, whereas cystoblasts require the bam and bgcn genes. Bam is especially attractive as a target of GSC differentiation factors because current evidence indicates that bam is both necessary and sufficient for cystoblast differentiation. In this paper, we have sought to distinguish between mutually exclusive transcriptional or post-transcriptional mechanisms as the primary regulators of bam expression in GSCs and cystoblasts. We find that bam transcription is active in young germ cells but is repressed specifically in GSCs. Activation depends on a 50 bp fragment that carries at least one germ cell-specific enhancer element. A non-overlapping 18 bp sequence carries a transcriptional silencer that prevents bam expression in the GSC. Promoters lacking this silencer cause bam expression in the GSC and concomitant GSC loss. Thus, asymmetry of the GSC division can be reduced to identifying the mechanism that selectively activates the silencer element in GSCs.

A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell.

In Drosophila, male and female gametes begin development when a stem cell divides to produce a cyst precursor. Subsequently, four special divisions give rise to a cluster of 16 interconnected cystocytes that develop into a single egg or 64 sperm. We identified and characterized a gene, bag-of-marbles (bam), that disrupts cyst formation in both sexes. An apparent null mutation causes abnormal cysts to form containing an excess number of cells that cannot differentiate into gametes. bam function resides within a simple 2.2-kb transcription unit encoding a single 442-amino-acid protein that shows similarity to the product of the ovarian tumor gene. The specific expression of bam RNA within female cystoblasts suggested that it might be involved in the specific cell-cycle alterations that occur during cystocyte divisions.

/pdf/bag-of-marbles-a-drosophila-gene-required-to-initiate-both-4zadvy4lz2.pdf

bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis.

Stem cells divide asymmetrically, regenerating a parental stem cell and giving rise to a daughter cell with a distinct fate. In many stem cell lineages, this daughter cell undergoes several amplificatory mitoses, thus generating more cells that embark on the differentiation program specific for the given lineage. Spermatogenesis in Drosophila is a model system to identify molecules regulating stem cell lineages. Mutations at two previously identified loci, bag-of-marbles (bam) and benign gonial cell neoplasm (bgcn), prevent progression through spermatogenesis and oogenesis, resulting in the overproliferation of undifferentiated germ cells. Here we investigate how bam and bgcn regulate the male germline stem cell lineage. By generating FLP-mediated clones, we demonstrate that both bam and bgcn act autonomously in the germline to restrict proliferation during spermatogenesis. By using enhancer trap lines, we find that the overproliferating germ cells express markers specific to amplifying germ cells, while at the same time retaining the expression of some markers of stem cell and primary spermatogonial cell fate. However, we find that germ cells accumulating in bam or bgcn mutant testes most resemble amplifying germ cells, because they undergo incomplete cytokinesis and progress through the cell cycle in synchrony within a cyst, which are two characteristics of amplifying germ cells, but not of stem cells. Taken together, our results suggest that bam and bgcn regulate progression through the male germline stem cell lineage by cell-intrinsically restricting the proliferation of amplifying germ cells.

bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis

Gonial cell neoplasm of genetic origin affecting both sexes of drosophila melanogaster.

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Gonial cell neoplasm of genetic origin affecting both sexes of drosophila melanogaster.