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doi: 10.1242/10.1242/dev.00214

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Development of the Drosophila genital disc requires interactions between its segmental primordia

¹ Centro de Biologia Molecular `Severo Ochoa', C.S.I.C., Universidad Autonoma de Madrid, Cantoblanco, E-28049 Madrid, Spain
² Centro de Investigaciones Biológicas, C.S.I.C., Velázquez 144, 28006 Madrid, Spain

View larger version (25K): [in a new window]   Fig. 1. Development of the genital disc and adult derivatives in both sexes. The female and male genital discs are shown as ventral, dorsal and parasagittal views. A8 (female primordium, pink), A9 (male primordium, blue) and A10-11 (anal primordium, green) indicate the corresponding abdominal segments. The posterior compartment of each primordium is shown in darker colours (pink, blue and green). Note that each posterior compartment is adjacent to the anterior cells corresponding to its own segment and to the anterior cells of the following segment, as occurs in the abdomen (parasagittal view). The P compartment cells of the three segmental primordia converge in the lateral areas (asterisk) but not in the centre of the disc. A, anterior compartment; P, posterior compartment; FGP, female genital primordium; MGP, male genital primordium; AP, anal primordium; RFP, repressed female genital primordium; RMP, repressed male genital primordium. External female terminalia: dAp, dorsal anal plate; vAp, ventral anal plate; T8, tergite eight; dVu, dorsal vulva; vVu, ventral vulva; dVp, dorsal vaginal plate; vVp, ventral vaginal plate. Internal female terminalia: U, uterus; Sr, seminal receptacle; Spt, spermatheca; Pov, parovaria; Od, oviduct (connected to the ovaries). Male external terminalia: Ap, anal plate; Ga, genital arch; Ll, lateral lobe; Lp, lateral plate; Cl, clasper; PA, penis apparatus. Internal male terminalia: Ed, ejaculatory duct; Sp, sperm pump; Pg, paragonia (male accessory gland); Vdef, vas deferens (connected to the testes). Modified, with permission, from Epper and Nöthiger (Epper and Nöthiger, 1982) and P. C. Ehrensperger (PhD thesis, University of Zürich, Switzerland, 1983).

View larger version (124K): [in a new window]   Fig. 2. Hh from posterior compartment cells signals to anterior cells both infront and behind as shown by Ptc expression in male and females. (A-D) Ptc (green) and hh-lacZ (red) expression in male (A,B) and female (C,D) genital discs. The segmental primordia corresponding to each genital primordium are indicated on the right side of each panel. The broken line separates the different genital primordia in each disc. Expression of ptc induced by Hh at the segmental border (arrows) and parasegmental borders (arrowheads). (E) Expression of Cad (red) and Ptc (green) in the A10-11 segment. In the analia, Cad is expressed in a gradient (double arrows) in the most anterior part of the A10-11 segment. (F,G) This new band of ptc expression (F) overlaps with the lowest intensity level of the cad expression gradient (G) in the analia.

View larger version (50K): [in a new window]   Fig. 3. En expression in the posterior A9 extends to the anterior A10-11. (A) En (green) and Hh (red) expression in A9 and A10-11 segmental primordia (AP) in the male genital disc. En expression in the posterior compartment of A9 segment extends to the A10-11 segment in a graded manner (double arrow, B). (C) En (green) and Cad (red) expression in A9 and A10-11 segmental primordia (AP) in the male genital disc. En and Cad expression overlap in the most anterior cells of the A10-11 segment. A gradient of both En and Cad expression is observed (double arrow) in the overlapping region (D). Hh expression therefore defines the border between segments A9 and A10.

View larger version (92K): [in a new window]   Fig. 4. Hh signal from posterior A9 induces En and Ptc expression in the most anterior part of A10-11. (A,B) Overexpression of Hh in the En domain of A9 using en-Gal4/UAS-hh expands (double arrow) Ptc (green, A) and En (green, B) expression and causes a reduction (double arrow) in Cad (red) expression in the most anterior part of A10-11. (C,D) smo- clones (which do not receive the Hh signal) in the most anterior part of A10-11 segment fail to express either Ptc (C) or En (D). A10-11 is labelled by the expression of Cad (blue). The smo- clones (thicker outline) and associated twin cells (thinner outline) are marked by ß-gal (C) or GFP (D) expression (green).

View larger version (134K): [in a new window]   Fig. 5. Cell lineage restriction in dsx1 intersexual genital discs. (A,B) ß-Gal-expressing clones (red) in dsx1 intersexual genital discs induced at 0-24 hours of development. (A) A ß-gal-expressing clone in the A8 segment that does not cross to the A9 segment. To distinguish the segmental border between male and female genital primordia, we used an antibody against Teashirt (green) that is specifically expressed in the A8 abdominal segment (female genital primordium). (B) Clones in A9 do not cross to A10-11. We used the anti-Cad antibody (green) to distinguish the segmental border between the male primordium and the anal primordium.

View larger version (63K): [in a new window]   Fig. 6. The cell-lineage restriction border between segments A9 and A10-11. (A,B) Several samples of smo- clones induced in the region around the segmental border between segments A9 and A10-11. Clones (thinner outline) and their sister twins (thicker outline) are marked by GFP expression. The segmental border is marked by hh-lacZ expression. Clones 1 and 2 (A) are induced in the P compartment of A9, and clones 3 (A) and 4 (B) are located in the anterior compartment of A10-11. (C) smo cad double mutant clones (5 and 6) induced in the anterior region of A10-11. Note that 3, 4, 5 and 6 clones abut but do not straddle the segmental border between A9 and A10-11. See schemes on the right of the figure to locate the clones in the genital discs. 1'-6' indicate the corresponding twin clones.

View larger version (121K): [in a new window]   Fig. 7. Diffusion of Hh signal across segmental borders. (A-D) Ectopic Hh expression in the anal primordium in the cad-Gal4/UAS-hh combination duplicates genital structures both in females and males. (A,B) Wild-type structures of the female and male external terminalia. (C,D) Duplicated male genital disc UAS-hh/cad-Gal-4. (E,F) Duplicated male genital discs stained with anti-Wg (green) and anti-Cad (red). Ventral section (E) and dorsal section (F) of the same disc. vVp, ventral vaginal plate; dVp, dorsal vaginal plate; dAp, dorsal anal plate; vAp, ventral anal plate; T8, tergite eight; GA, genital arch; Ap, anal plate; Ad, apodeme; Lp, lateral plate; Cl, clasper; PA, penis apparatus; Hy, hypandrium; Vp', vaginal plates; Ad', Hy'; Vp'; PA' are the duplicated structures. MGP, male genital primordium.

View larger version (162K): [in a new window]   Fig. 8. Diffusion of Wg and Dpp signals across segmental borders. (A) The terminalia of dppd5/dppd12 mutant males is very much reduced. Note the triplication of penis apparatus structures (asterisk) and the apodeme (arrowhead). (B) Ectopic dpp clones induced 24-48 hours after egg laying (indicated by a dotted line) non-autonomously recover the whole inventory of external genital structures, with the exception of one lateral lobe structure. (C) Phenotype of Sp/wgcx3 females with reduced vaginal plates and no vulva. In this mutant background, overexpression of Wg in the Cad domain (D) duplicates the vaginal plates (arrow). (E) Phenotype of Sp/wgcx3 males with no penis apparatus structures, and reduced claspers plus fused lateral plates (asterisk). Note the duplication of the lateral plate. In this mutant background, overexpression of Wg in the Cad domain (F) recovers the claspers (arrowhead) and some penis apparatus structures (arrow).

View larger version (75K): [in a new window]   Fig. 9. Effect of ablation of the genital and anal primordium cells on the development of the genital disc. (A,B) Lack of terminal structures of female (A) and male (B) cad-GAL4; UAS-ricin, UAS-lacZ adults. (C) A very reduced cad-GAL4; UAS-ricin, UAS-lacZ genital disc. The anal primordium is labelled with anti-Cad antibody (in red). (D,E) Male genital discs expressing the cold-sensitive Ricin mutant protein in A8 (repressed female genital primoridum) using the tsh-GAL4 line at the restrictive temperature (D) where the Ricin protein is not functional, and (E) at the permissive temperature. The discs are stained with anti-ß-gal (in red) to label the A8 segment and with anti-Distal-less (in green) antibodies. Note the small size of the genital disc expressing functional Ricin protein in A8 and the lack of Distal-less expression in A9 (male genital primordium). Broken lines separate the three segmental primordia of the genital disc. T5, tergite 5; T6, tergite 6; T7, tergite 7.