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First published online November 3, 2003
doi: 10.1242/10.1242/dev.00804


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Mechanisms of germ cell specification across the metazoans: epigenesis and preformation

Cassandra G. Extavour* and Michael Akam

Laboratory for Development and Evolution, University Museum of Zoology, Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK



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Fig. 1. Germ cell specification in model systems. (A) A cellular blastoderm stage D. melanogaster embryo stained with anti-Vasa antibody. The pole cells (arrowhead), located at the posterior pole of the embryo, are the primordial germ cells (PGCs), and express vasa protein. (B) Mouse embryo at 7 dpc stained with alkaline phosphatase. Enzymatic activity is high in the PGCs (arrowhead), which are located in the proximal epiblast at the base of the allantois [Reproduced with permission from McLaren (McLaren, 2003Go)]. Anterior is to the left in both panels.

 


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Fig. 2. Examples of germ cell identification in non-model systems. (A) An adult Mnemiopsis leidyi (a comb jelly of the phylum Ctenophora) in which germ cells seem to arise by epigenesis. These hermaphrodites have eight rows of gonads, each gonad containing an ovary and a testis behind each of the eight rows of comb plates (also called ctene rows) (asterisks). (B) Close up of area boxed in A. Germ cells are first identified in ctenophores after the larvae hatch, next to the meridional canals that give rise to the ctene rows. Multiple ovaries (black arrowheads) and testes (white arrowheads) develop on either side of the canals. In this panel, eggs (asterisks) are being extruded through the gonoducts. (C) Juvenile Blatta germanica cockroach (phylum Arthropoda). Germ cells in these insects do not appear to be determined by preformation. (D) The embryonic rudiment of B. germanica forms on the surface of the yolk (yellow). (D, part i) Germ cells (gz) are first identified at the posterior of the germ band, after formation of the mesoderm (ms). (ii) As development proceeds, germ cells continue to arise from the mesoderm of the coelomic sacs (c), which are being formed in each segment in an anteroposterior progression. (iii) The number of germ cells increases, and they populate the coelomic sacs of the segments from which the gonad will form. c, coelomic sac; ek, ectoderm; gz, germ or reproductive cells (genitalzellen); ms, mesoderm; st, stomodaeum (Heymons, 1891Go). (E) A copepod of the genus Cyclops (phylum Arthropoda). All copepods that have been studied segregate germ cells by preformation. (F) Embryonic cleavages of Cyclops fuscus are holoblastic and equal. (i) In the first cleavage, dense granular material associates with only one of the centrosomes. (ii) The resulting two-cell stage has the granular material in only one of the blastomeres (orange). (iii) The granular material continues to be asymmetrically segregated to a single blastomere (orange) in subsequent cleavages. (iv) At the time of gastrulation, the cell containing the granular cytoplasm has divided to give rise to two cells that are located at the tip of the invaginating archenteron, which are the PGCs (Ug: Urgeschlechtszellen) (Amma, 1911Go). (G) Late stage embryo of the turtle Trachemys scripta (phylum Chordata), stained with Alcian Blue for cartilage and Alizarin Red for bone. Reptiles seem to segregate germ cells epigenetically. (H, part i) Section of an embryo of the turtle Sternotherus odoratus at the three somite stage. Germ cells are first identified at this stage of development, in two zones (Z) lateral to the neural groove (NG). (ii) Close up of area boxed in i. PGCs in the germ cell zone (Z) are distinguishable from somatic cells of the ventral ectoderm (VE) as large cells with round nuclei and granular cytoplasm. AC, amnion and chorion; DE, definitive endoderm; N, notochord; NG, neural groove; VE, vitelline endoderm; Z, germ cell zone. Reproduced with permission from Risley (Risley, 1933Go). Scale bars: 3 mm in A; 250 µm in B; 150 µm in C; 50 µm in E; 5 mm in G.

 


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Fig. 3. Modes of germ cell specification across the Metazoa. Boxes refer to modes of germ cell specification as described in the existing literature: red, epigenesis; blue, preformation; half red, half blue, groups in which some species show preformation and others epigenesis; white, no data. Asterisks indicate phyla in which epigenesis has been claimed, but recent data suggest preformation (see discussion in main text). Phylogeny is modified from Peterson and Eernisse (Peterson and Eernisse, 2001Go), but many relationships within the Ecdysozoa and Lophotrochozoa remain unresolved by molecular data (Adoutte et al., 2000Go). The phylogenetic positions of the Chaetognatha and Gnathostomulida are particularly uncertain (dotted lines).

 





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