Abstract

Gametes are highly specialized cell types produced by a complex differentiation process. Production of viable oocytes requires a series of precise and coordinated molecular events. Early in their development, germ cells are an interconnected group of mitotically dividing cells. Key regulatory events lead to the specification of mature oocytes and initiate a switch to the meiotic cell cycle program. Though the chromosomal events of meiosis have been extensively studied, it is unclear how other aspects of oocyte specification are temporally coordinated. The fruit fly, Drosophila melanogaster, has long been at the forefront as a model system for genetics and cell biology research. The adult Drosophila ovary continuously produces germ cells throughout the organism’s lifetime, and many of the cellular processes that occur to establish oocyte fate are conserved with mammalian gamete development. Here, we review recent discoveries from Drosophila that advance our understanding of how early germ cells balance mitotic exit with meiotic initiation. We discuss cell cycle control and establishment of cell polarity as major themes in oocyte specification. We also highlight a germline-specific organelle, the fusome, as integral to the coordination of cell division, cell polarity, and cell fate in ovarian germ cells. Finally, we discuss how the molecular controls of the cell cycle might be integrated with cell polarity and cell fate to maintain oocyte production.

Highlights

  • Successful sexual reproduction requires high-quality haploid gametes

  • The discovery that homologous chromosome pairing occurs prior to meiotic entry suggests that they are tightly linked processes, oocyte selection can be uncoupled from premeiotic events

  • How cyst divisions are coordinated with meiotic entry and the timing of oocyte selection is an important topic for further study

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Summary

Introduction

Successful sexual reproduction requires high-quality haploid gametes. In many organisms, germ cells (which produce gametes) initially divide mitotically to form clusters of germ cells, from which differentiated oocytes or sperm arise. The second model of oocyte specification suggests that the oocyte is specified at the time of the first mitotic division of the cystoblast, establishing an asymmetry that is maintained in subsequent mitoses (Figure 5C) (Yue and Spradling, 1992; Lin et al, 1994; Theurkauf, 1994a; de Cuevas and Spradling, 1998).

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