Protecting and Diversifying the Germline

Abstract

Gametogenesis represents the most dramatic cellular differentiation pathways in both female and male flies. At the genome level, meiosis ensures that diploid germ cells become haploid gametes. At the epigenome level, extensive changes are required to turn on and shut off gene expression in a precise spatiotemporally controlled manner. Research applying conventional molecular genetics and cell biology, in combination with rapidly advancing genomic tools have helped us to investigate (1) how germ cells maintain lineage specificity throughout their adult reproductive lifetime; (2) what molecular mechanisms ensure proper oogenesis and spermatogenesis, as well as protect genome integrity of the germline; (3) how signaling pathways contribute to germline-soma communication; and (4) if such communication is important. In this chapter, we highlight recent discoveries that have improved our understanding of these questions. On the other hand, restarting a new life cycle upon fertilization is a unique challenge faced by gametes, raising questions that involve intergenerational and transgenerational epigenetic inheritance. Therefore, we also discuss new developments that link changes during gametogenesis to early embryonic development—a rapidly growing field that promises to bring more understanding to some fundamental questions regarding metazoan development.

Coordinating Proliferation, Polarity, and Cell Fate in the Drosophila Female Germline

“…In the anterior half of the germarium, cysts arise from the mitotic expansion of GSCs and their differentiating daughters (Figures 2D, 3). GSCs divide mitotically with asymmetric division, giving rise to two cells of unequal fates: a new stem cell and a cystoblast destined for differentiation (Schüpbach et al, 1978;Wieschaus and Szabad, 1979;Lin and Spradling, 1993;reviewed in: Xie, 2013;Gleason et al, 2018;Drummond-Barbosa, 2019;Kahney et al, 2019). The cystoblast undergoes exactly four rounds of mitotic division with incomplete cytokinesis, creating interconnected 2, 4, 8, and 16 cell cysts (King, 1970;Spradling, 1993).…”

Drosophila MARF1 ensures proper oocyte maturation by regulating nanos expression

“…Drosophila melanogaster is an ideal model organism for the detailed study of oogenesis. Drosophila females have one pair of ovaries that consist of 18-20 ovarioles (reviewed in [1][2][3]). In germarium-a structure at the anterior tip of the ovariole-two or three germline stem cells (GSCs) are maintained in the undifferentiated status in a niche environment.…”

Diversity of piRNA expression patterns during the ontogeny of the German cockroach

“…The RNAi system of the insect last common ancestor diversified and expanded through time across the different insect lineages (Dowling et al., ). Although the canonical functions of piRNAs are associated with genome protection from transposon activity during embryogenesis, evidences of additional roles (like regulation of gene expression) are growing (Gebert, Ketting, Zischler, & Rosenkranz, ; Gleason et al., ; Le Thomas et al., ; Lewis et al., ; Peng & Lin, ; Pritykin, Brito, Schupbach, Singh, & Pane, ; Sarkar, Volff, & Vaury, ). As the taxonomic spectrum of studied species broadens, the complexity of the piRNA system appears to expand.…”

“…The piRNA transcription does not seem to occur through canonical promoters. It has been proposed that the Rhino‐Deadlock‐Cutoff (RDC) complex would participate in regulating the transcription of piRNA clusters in germ cells, inhibiting the transcription of adjacent genes in the cluster or allowing the functionality of noncanonical promoters (Gleason, Anand, Kai, & Chen, ). Moreover, the localization of some piRNA clusters in heterochromatic regions led to the study of them in relation to histone modifications, which has revealed an important role of H3K9me3 on cluster transcription (Mohn, Sienski, Handler, & Brennecke, ; Molla‐Herman, Vallés, Ganem‐Elbaz, Antoniewski, & Huynh, ).…”

“…Moreover, the localization of some piRNA clusters in heterochromatic regions led to the study of them in relation to histone modifications, which has revealed an important role of H3K9me3 on cluster transcription (Mohn, Sienski, Handler, & Brennecke, ; Molla‐Herman, Vallés, Ganem‐Elbaz, Antoniewski, & Huynh, ). In somatic cells, the mechanisms regulating piRNA transcription are less known, but it has been suggested that the control exerted by the RDC complex would not be necessary in these cells (see Gleason et al, ).…”