ABSTRACT
Stem cell behavior is regulated by extrinsic signals from specialized microenvironments, or niches, and intrinsic factors required for execution of context-appropriate responses to niche signals. Here we show that function of the transcriptional regulator longitudinals lacking (lola) is required cell autonomously for germline stem cell and somatic cyst stem cell maintenance in the Drosophila testis. In addition, lola is also required for proper execution of key developmental transitions during male germ cell differentiation, including the switch from transit amplifying progenitor to spermatocyte growth and differentiation, as well as meiotic cell cycle progression and spermiogenesis. Different lola isoforms, each having unique C-termini and zinc finger domains, may control different aspects of proliferation and differentiation in the male germline and somatic cyst stem cell lineages.
Subject(s)
Cell Differentiation , Drosophila Proteins/metabolism , Drosophila melanogaster/cytology , Drosophila melanogaster/genetics , Spermatozoa/cytology , Stem Cells/cytology , Testis/cytology , Transcription Factors/metabolism , Animals , Cell Differentiation/genetics , Cell Division , Cell Lineage/genetics , Drosophila Proteins/genetics , Gene Expression Regulation, Developmental , Gene Knockdown Techniques , Janus Kinases/metabolism , Male , Meiosis , Mutation/genetics , Nuclear Proteins/genetics , Nuclear Proteins/metabolism , Protein Isoforms/genetics , Protein Isoforms/metabolism , RNA Interference , STAT Transcription Factors/metabolism , Signal Transduction , Spermatogenesis/genetics , Spermatogonia/cytology , Spermatogonia/metabolism , Spermatozoa/metabolism , Stem Cells/metabolism , Transcription Factors/genetics , Transforming Growth Factor beta/metabolismABSTRACT
Adult stem cells are believed to be maintained by a specialized microenvironment, the niche, which provides short-range signals that either instruct stem cells to self-renew or inhibit execution of preprogrammed differentiation pathways. In Drosophila testes, somatic cyst stem cells (CySCs) and the apical hub form the niche for neighboring germline stem cells (GSCs), with CySCs as the proposed source of instructive self-renewal signals [Leatherman JL, Dinardo S (2010) Nat Cell Biol 12(8):806-811]. In contrast to this model, we show that early germ cells with GSC characteristics can be maintained over time after ablation of CySCs and their cyst cell progeny. Without CySCs and cyst cells, early germ cells away from the hub failed to initiate differentiation. Our results suggest that CySCs do not have a necessary instructive role in specifying GSC self-renewal and that the differentiated progeny of CySCs provide an environment necessary to trigger GSC differentiation. This work highlights the complex interaction between different stem cell populations in the same niche and how the state of one stem cell population can influence the fate of the other.
Subject(s)
Cell Differentiation , Cell Lineage , Drosophila melanogaster/cytology , Germ Cells/cytology , Stem Cells/cytology , Testis/cytology , Animals , Drosophila melanogaster/metabolism , Germ Cells/metabolism , Male , Signal Transduction , Stem Cells/metabolism , Transforming Growth Factor beta/metabolismABSTRACT
It is generally considered that meiotic recombination rates increase with temperature, decrease with age, and differ between the sexes. We have reexamined the effects of these factors on meiotic recombination in the nematode Caenorhabditis elegans using physical markers that encompass >96% of chromosome III. The only difference in overall crossover frequency between oocytes and male sperm was observed at 16 degrees . In addition, crossover interference (CI) differs between the germ lines, with oocytes displaying higher CI than male sperm. Unexpectedly, our analyses reveal significant changes in crossover distribution in the hermaphrodite oocyte in response to temperature. This feature appears to be a general feature of C. elegans chromosomes as similar changes in response to temperature are seen for the X chromosome. We also find that the distribution of crossovers changes with age in both hermaphrodites and females. Our observations indicate that it is the oocytes from the youngest mothers-and not the oldest-that showed a different pattern of crossovers. Our data enhance the emerging hypothesis that recombination in C. elegans, as in humans, is regulated in large chromosomal domains.
