~EVIEWS 6 Hiilskamp, M., Pfeifle, C. and Tautz, D. (1990) Nature 346, 577-580 7 Green, J.B.A. (1990) BioEssalJs 12, 437--439 8 Eichele, G. (1989) Trends Genet. 5, 246-251 9 Brockes, J. (199l) Nature 350, 15 10 Ruiz i Altaba, A. and Melton, D.A. (1990) Trends Genet. 6, 57-64 11 Nieuwkoop, P.D. (1973) Adv. Morphol. 10, 1-39 12 New, H.V. and Smith, J.C. (1990) Curr. Opin. Cell Biol. 2, 969-974 13 Smith, J.C. (1989) Development 105,665-677 14 Asashima, M. et al. (1990) Wilhelm Roux's Arch. Dev. Biol. 198, 330-335 15 Smith, J.C., Price, B.M,, Van, N.K. and Huy[ebroeck, D. (1990) Nature 345, 732-734 16 van den Eijnden Van Raaij, A.J. et al. (1990) Nature 345, 819-822 1 7 Thomsen, G. et al. (1990) Cell 63, 485-493 18 Wolpert, L. (1989) in The Molecular Basis of Positional Signalling (Development Supplement) (Kay, R. and Smith, J., eds), pp. 3-12, Company of Biologists 19 Green, J.B.A. etal. (1990) Development 108, 229-238 20 Green, J.B.A. and Smith, J.C. (1990) Nature 347, 391-394 21 Struhl, G., Struhl, K. and Macdonald, P.M. (1989) Cell 57, 1259-1273 22 Driever, W., Thoma, G. and Niisslein-Volhard, C, (1989) Nature 340, 363-367 23 Lewis, J.H., Slack, J.M.W. and Wolpert, L. (1977),L Theor. Biol. 65, 579-590 24 Goldbeter, A. and Wolpert, L. (1990)J. Theor. Biol. 142, 243-250 25 Gurdon, J.B. (1988) Nature 336, 772-774 26 Rosa, F.M. (1989) Cell 57, 965-974 27 Slack, J.M.W. (1991) Nature 349, 17-18

T h e differentiation of distinct cell types is the result of changes in the patterns of gene expression in precursor cells. These patterns are largely regulated by changes in the activities of the pool of transcription factor proteins, and different cell types may be maintained by the expression of different sets of such factors. However, developmental changes of cell type must begin with the modulation of the activities of pre-existing transcription factors. Thus to understand development we must understand how inductive signals from outside a target cell modulate the transcription factor activities within it. The Drosophila adult compound eye consists of about 800 similar facets, or ommatidia, each comprising eight neuronal photoreceptor cells [six outer cells (R1-6) and two different inner cells (R7 and R8)] and 12 accessory cells 1--~ (Fig. 1). The eye develops from an unpatterned monolayer epithelium (the eye imaginal disc), beginning in the third larval instar when a transverse indentation, the morphogenetic furrow, begins to move across the eye field from posterior to anterior 1-5 (Fig. 1). Behind the furrow, the cells of the developing ommatidia are thought to be assembled by the sequential induction of multipotent precursor cells through inductive signals from their predecessors, beginning with the-photoreceptor cells. There are three categories of evidence for the sequential induction of the ommatidial cells; considered as a

28 Ellinger-Ziegelbauer, H. and Dreyer, C. (1991) Genes Dev. 5, 94--104 29 Musci, T.J., Amaya, E. and Kirschner, M.W. (1990) Proc. Natl Acad. Sci. USA 87, 8365-8369 30 Gillespie, L.L., Paterno, G.D. and Slack, J.M. (1989) Development 106, 37-46 31 Stern, C.D. and Canning, D.R. (1990) Nature 343,

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21-30 36 Weeks, D.L. and Melton, D.A. (1987) Proc. NatlAcad. Sci. USA 84, 2798--2802 37 Dale, L., Matthews, G., Tabe, L. and Colman, A. (1989) EMBOJ. 8, 1057-1065 38 Tannahill, D. and Melton, D.A. (1989) Development 106, 775-785 39 Mitrani, E. et al. (1990) Cell 63, 495-501 40 Dale, L. and Slack, J.M. (1987) Development 99, 527-551 41 Crick, F.H.C. (1970) Nature 225, 420--422 42 Cooke, J. (1983) J. Embryol. Exp. Morpbol. 76, 95-104 43 Green, J.B.A. and Cooke, J. Semin. Dev. Biol. (in press) 44 Smith, J.C. (1981)J. Embryol. Exp, Morphol. 65 (Suppl.), 187-207 .].B.A. GREENANDJ.C. SMITHAREIN THENATIONALINSTITUTE FORMEDICALRESEARCH,THERIDGEWAY,MILLHILL, LONDON NW7 IAA, UK.

The r01e of transcription factors in the developing Drosophilaeye KEVIN MOSES In the developing Drosophila compound eye, multipotent precursor cells are induced to develop into particular cell types through sequential induction. In the target cells, transcription factors may be modulated by the inductive signals to execute their instructions. Four recentlF isolated genes may encode such developmentally modulated transcription factors. whole, the evidence is compelling. (1) An alternative, lineage-directed model 6 has been discounted by genetic mosaic experiments 1,7,~. (2) A precise and reproducible sequence of specific contacts is established and maintained between the developing ommatidial cells 2.9. The morphology of these cell contacts suggests they may be involved in a process of inductive signalling. (3) The discovery of cell homeotic genes (e.g. sevenless and bride ofsevenless) for which both genetic mosaic data 1°-12 and molecular data 13Ai' support functions as cell surface receptors and ligands.

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FSGH Development and structure of the Drosophila compound eye. A larval eye antennal imaginal disc is shown at the end of the third larval instar, with anterior (A) down and posterior (P) tip. The antenna1 (ANT) precursor lies anterior to the eye (EYE) field, which is connected to the brain by the optic stalk (OS). The morphogenetic furrow (MF, see text) has progressed about half way across the eye field, moving from posterior to anterior. One area has been expanded to show, some of the sequential events of the first ~30 h of ommatidial assembly. Six of -18 columns (or stages) are shown; the intermediate columns have been omitted for clarity. Tile youngest ommatidium is closest to the furrow (-2 h post-furrow), at which stage only one cell (the R8 precursor, sho\~n :is a filled ellipse) is a neuron (by antigenic and morphological criteria). At the second stage shown (-6 h post-furrow) three cells ha~u become neurons (the RS, R2 and R5 precursors). At the third stage shown (~12 h post-furrow) five cells have become neurons Ithu R8, R2, R5, R3 and R4 precursors). At the fourth stage shown (~18 h post-furrow) seven cells have become neurons (the RS. R2, R~,, R3, R4, R1 and R6 precursors). At the fifth stage shown (~26 h post-furrow) all eight photoreceptor cell precursors have become: neurons (R8, R2, RS, R3, R4, R1, R6 and R7) and the first two accessory cone cells are developing (shown as open ovals). At the last stage shown (-36 h post-furrow) ~ ' o more cone cells have joined. Development proceeds into pupal life as tlne other a(cessorv cells are added, and cell morphogenesis continues. The ommatidial cells do not arise from an immediate single precursor cell. hut rather by means of sequential induction (for reviews of these events see Refs 1-5). An adult ommatidium is shown in kmgitudinat section (right) and cross-section (left). In the longitudinal section the apical (AP) surface of the retina is tip, and the basal (BA) stir face is down. At the top right :ire the two cells of the hair-nerve group (hng). The lens (le) and crystalline cone (co) form the optical elements of the ommatidium. They are secreted by the cone cells (c) and focus light onto the photoreceptor cells (pc). The photoreceptor cells are long neuronal cells containing rhabdomeres (rh, rod-shaped photosensitive organelles) and they elaborate axons basally. The sheathing pigment cells :ire not drawn individually (for clarity) and are represented :is the shaded arca. An apical and basal cross-section are shown: the orientation is the same as tbr the developing larval ommatidia shown to the left. The rhabdomeres lie in a characteristic trapezoidal arrangement. There :ire six outer photoreceptor cells (RI%) with large rhabd

The role of transcription factors in the developing Drosophila eye.

In the developing Drosophila compound eye, multipotent precursor cells are induced to develop into particular cell types through sequential induction...
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