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The Control of Sexual Identity in the Drosophila Germline

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The Control of Sexual Identity in the Drosophila Germline REVIEW 2783 Development 133, 2783-2791 (2006) doi:10.1242/dev.02415 The control of sexual identity in the Drosophila germline Abbie Casper and Mark Van Doren* Whether to be male or female is a critical decision in Germline sex determination in Drosophila development. Nowhere is this more important than in the germ The establishment of sexual identity in the germline is thought to cells, which must produce either the sperm or eggs necessary occur differently from in the rest of the body (the somatic cells or for the perpetuation of the species. How does a germ cell make soma). In the soma, male versus female identity is regulated by the this decision and how is it executed? One thing that is clear is number of X chromosomes (or ratio of X chromosomes to that this process is very different in germ cells compared with autosomes), such that, in normal diploid animals, XX is female and other cells of the embryo. Here, we explore how sexual identity XY is male (Fig. 1) (reviewed by Cline and Meyer, 1996). The Y is established in the Drosophila germline, how this affects other chromosome is not important for sex determination in either the aspects of germ cell development and what studies in soma or the germline in Drosophila, but does contain genes that Drosophila can teach us about mammalian germ cells. are required for spermatogenesis. In the soma, XX embryos activate expression of Sex-lethal (Sxl), which functions through Introduction Animals have evolved a fascinating array of mechanisms for conducting sexual reproduction, including those used for attracting Box 1. A glossary of terms a mate, courting a mate and getting the gametes together. These mechanisms often differ drastically between different species. Sexual dimorphism However, one thing that all sexual animals have in common is the Any difference in the characteristics (phenotype) of an otherwise production of distinct male and female gametes that must unite to equivalent cell type, in males versus females. This includes a sex- initiate development of a new individual. Thus, the study of how a specific pattern of gene expression, as well as any other aspects of sex-specific development. germ cell is guided along a male or female path, to eventually produce either sperm or eggs, is central to our understanding of Sexual identity sexual reproduction and fertility. A difference in identity or developmental potential of an otherwise In this review, we discuss germline sexual identity within the equivalent cell type, in males versus females. Any sexual dimorphism context of the different stages of germline sexual development and in a cell type, even the expression of a single sex-specific gene, can the decisions that germ cells face along the way (see Box 1 for a indicate that sexual identity has been initiated. However, sexual discussion of terms). This includes the process of germline sex identity may also require maintenance, and a cell may receive determination, by which a germ cell acquires a male versus additional sex-specific inputs that influence sexual identity. This may be particularly true in the germline, where continued interactions female identity, but also how sexual identity influences other between the soma and germline influence all aspects of germ cell events, such as the formation of male or female germline stem development. cells and entry into spermatogenesis or oogenesis. Although germline sex determination and sexual development have not Sex determination always been studied together, it is clear that we cannot understand The mechanism by which a cell, or organism, acquires its sexual one without the other. An understanding of germline sex identity. In some cell types, this may involve a single event that determination depends on our understanding how the irreversibly establishes a male versus female identity. In other cell developmental paths of male and female germ cells diverge. types, sex determination may be an ongoing process with multiple stages of commitment. Similarly, understanding other events in male versus female germ cell development requires an understanding of the role germ cell Sexual differentiation sexual identity plays in these processes. Therefore, we first How a cell or tissue uses its sexual identity to produce a sex-specific discuss work on germline sex determination that has contributed phenotype (sexual dimorphism). However, this term can be confusing greatly to our knowledge of how this process is controlled. We for the germline because, even though the formation of male versus then discuss our emerging understanding of germ cell sexual female germline stem cells is an interesting sexual dimorphism, development and how this affects our thinking about germline sex germline stem cells are still considered to be in a relatively determination. Finally, we briefly discuss how understanding ‘undifferentiated’ state. Thus, we will only use the term sexual differentiation to refer to the processes of spermatogenesis or these events in Drosophila can shed light on similar events in oogenesis. mammalian germ cell development and human fertility. As this represents several distinct subjects, each of which is worthy of an Sexual development entire review, we have, by necessity, focused on specific findings This term encompasses all aspects of sex-specific development, from T and refer readers to more-comprehensive reviews on related the time a cell first establishes its sexual identity through the process topics, where appropriate. of sex-specific terminal differentiation. In the germline, this would include the earliest aspects of germ cell sexual dimorphism in the embryonic gonad, through the formation of male or female germline stem cells and the ultimate production of sperm or eggs. Although this may seem a broad term, it emphasizes the thinking that the Department of Biology, 302 Mudd Hall, Johns Hopkins University, 3400 North different aspects of sex-specific germ cell development are Charles Street, Baltimore, MD 21218, USA. interrelated and cannot be readily understood in isolation. *Author for correspondence (e-mail: [email protected]) DEVELOPMEN 2784 REVIEW Development 133 (15) XX but mutant for tra develop as males (Sturtevant, 1945), including Somatic gonad a male somatic gonad. However, as tra is not required in the X:A germline, this results in XX germ cells developing in a male soma, Germ cell Sxl similar to the transplant experiments described above. X:A Overexpression of tra is sufficient to feminize an XY soma tra tra2 ovo (McKeown et al., 1988), creating the opposite situation. otu dsx Male germ cells in a female soma Sxl When XY germ cells develop in a female soma [using the above Jak/Stat methods and others; see Oliver (Oliver, 2002), for an extensive review], the result is often an ‘ovarian tumor’, where germline cysts in the ovary contain tens to hundreds of small individual Upd germ cells instead of 15 interconnected nurse cells and an oocyte, as in a normal ovarian cyst. At times, these germ cells appear unambiguously male with characteristics of differentiating spermatocytes (Steinmann-Zwicky et al., 1989), indicating that Fig. 1. A simplified view of sex determination pathways in the somatic gonad and germline. In somatic cells, the ratio of X XY germ cells can retain a male identity in a female soma. chromosomes to autosomes (X:A) influences the activity of Sex-lethal However, characteristics of oogenesis can also be observed in (Sxl), which, in turn, activates transformer (tra). tra, along with these experiments (Nagoshi et al., 1995; Waterbury et al., 2000) transformer 2 (tra2), controls the alternative RNA splicing of doublesex and analyses using molecular markers reveal that these germ (dsx), which determines whether the somatic gonad will develop as cells have both male and female characteristics (Hinson and male or as female. In the germ cells, the X:A ratio also influences sexual Nagoshi, 1999; Janzer and Steinmann-Zwicky, 2001; Waterbury identity, and ovo, ovarian tumor (otu) and Sxl promote female germ cell et al., 2000). Furthermore, XY germ cells do not always survive development. Interactions between germ cells and somatic cells also in a female environment (Schüpbach, 1985; Steinmann-Zwicky et influence germline sex determination and act through extracellular al., 1989). Thus, although the ovarian tumor phenotype is ligands, such as Unpaired (Upd), which promotes male development. commonly observed, and is likely a result of XY germ cells Gap junctions (red) may also facilitate communication between the two cell types. maintaining aspects of male identity in a cell-autonomous manner, these germ cells are not fully male, and may also have compromised viability. transformer (tra) and transformer 2 (tra2) to regulate the splicing of doublesex (dsx) RNA, producing a female form of this Female germ cells in a male soma transcription factor. In XY animals, this pathway is off and a male XX germ cells are likely to fail to proliferate or to die when present form of DSX is produced by default. dsx regulates male versus in a male soma. XX germ cells transplanted into a male soma are female development in most somatic cells, including the somatic recovered at a greatly reduced frequency relative to the reciprocal gonad, while in the nervous system, a second target for this transplantation (Steinmann-Zwicky, 1993; Steinmann-Zwicky et pathway, fruitless, regulates most aspects of sex-specific behavior al., 1989). Similarly, in XX animals where the soma has been (Ryner et al., 1996). As we discuss below, the rules for determining
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