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WIREs Dev Biol
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Vertebrate female germline—the acquisition of femaleness

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The cellular and molecular characteristics of female germ cells have primarily been studied in the mammalian ovary. In most female mammals, all primordial germ cells (PGCs) develop into oocytes early during ovary formation, and germline stem cells are few in number or absent in postnatal ovaries (Lei L, Spradling AC. Female mice lack adult germ‐line stem cells but sustain oogenesis using stable primordial follicles. Proc Natl Acad Sci USA 2013, 110:8585–8590). Research efforts in the field have largely focused on meiosis and follicular development, but a fundamental question regarding establishment of femaleness, which is very important to understand the ‘female’ germline, has not been discussed sufficiently. Recent work has revealed the presence of germline stem cells in the vertebrate ovary, using the teleost fish, medaka (Oryzias latipes) (Nakamura S, Kobayashi K, Nishimura T, Higashijima S, Tanaka, M. Identification of germline stem cells in the ovary of teleost medaka. Science 2010, 328:1561–1563). This discovery allows direct comparison between female and male germline stem cells and raises an interesting and heretofore unaddressed issue regarding femaleness of germline stem cells. In this article, the germ cell behavior in the ovaries of different species is reviewed and compared, the molecular mechanisms underlying the generation of female germ cells are discussed, and the relationship between female germ cells and the surrounding somatic cells is examined. This article is categorized under: Early Embryonic Development > Gametogenesis Adult Stem Cells, Tissue Renewal, and Regeneration > Tissue Stem Cells and Niches Comparative Development and Evolution > Organ System Comparisons Between Species

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Schematic diagram comparing female (upper panel) and male (lower panel) gametogenesis. In female gonads, germ cells initially increase in number via type I division (maintenance type), then some cells switch to type II division (gematogenesis type) to form germline cysts. In the cysts, germ cells divide synchronously and are interconnected by intercellular bridges. In the mammalian ovary, all germ cells proceed along the shaded pathway during early ovarian development, such that only a pool of follicles is present in the adult ovary, while germ cells undergoing both types I and II divisions are observed simultaneously in the medaka developing ovary. In medaka adult ovary, all the events proceed in the structure of germinal cradle representing ovarian niche. Roman numerals indicate the possible stages at which germ cells may acquire femaleness. In male gonads, basically the same events occur, but at later stages, suggesting that early expression of meiosis markers is not equivalent to manifestation of femaleness.
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Common features in female and male gametogenesis. (1) Germline stem cells reside in cord‐like structures, ovarian cords in medaka and seminiferous tubules in mammals. (2) Germ cells are motile in the cord, implying some dynamic mechanism to regulate production of gametes. (3) Germline stem cells are surrounded by sox9‐expressing cells (blue cells indicated with arrows). (4) Gametogenesis proceeds in cord‐structures until meiotic prophase I from germline stem cells.
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Expression of sox9b in the medaka adult testis. A double transgenic medaka testis with sox9b (red) and nanos2 (green) fluorescent reporter expressions is shown. Spermatogenesis proceeds as units of lobules from right (distal) to left (proximal). Sertoli cells with high sox9b expression enclose nanos2‐expressing germline stem cell populations. Sertoli cells with lower sox9b expression enclose spermatocytes.
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Adult Stem Cells, Tissue Renewal, and Regeneration > Tissue Stem Cells and Niches
Early Embryonic Development > Gametogenesis
Comparative Development and Evolution > Organ System Comparisons Between Species