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doi: 10.1242/10.1242/dev.00187

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Genetic requirements of vestigial in the regulation of Drosophila wing development

Centro de Biología Molecular `Severo Ochoa'-Consejo Superior de Investigaciones Científicas, Universidad Autónoma de Madrid, Facultad de Ciencias, Madrid 28049, Spain

View larger version (103K): [in a new window]   Fig. 1. Cuticular transformations caused by the ectopic expression of vg (A,C) and co-overexpression of wgDN-vg (B,D) under the control of Dll-G4. Effects of vg ectopic overexpression on gene expression in the second pair of the legs driven by Dll-G4 (E-F). Lines indicate optical sections along the z-axis. Scale bars: 0.1 mm. (A) Ventral view of a transformed thorax with distal segments of first and second legs differentiating as wing blade (blue asterisk) and third legs as haltere (red asterisk). The broken red line separates anterior (a) from posterior (p) territories in transformed legs. (A1,A2) Transformed wing blade with dorsal (D) and ventral (V) regions. Arrowheads indicate veins. (A3) The arrowhead indicates a campaniform sensillae. (A4) Higher magnification of the wing margin in anteroposterior transition. (A5) Observe the histotypic differences between wing blade (blue asterisk) and haltere territories (red asterisk). (B) Ectopic co-expression of vg and a dominant-negative form of wg reduces the transformation phenotypes obtained with the ectopic expression of vg alone. (B1) Distal (D) (red arrowhead) and proximal (P) tarsal parts in the third pair of legs (red asterisk) at higher magnification. Distal segments (arrowhead indicates bracts) are shown in B2 and proximal segments (without bracts) in B3. (C) Ectopic expression of vg leads to transformation of antenna with anterior (a) and posterior (p) wing margin elements. The insets show the differentiation of wing margin elements with anterior (a; C1,C2) and posterior (p; C1,C2) specifications. (D) Transformation in the antenna is reduced by the co-expression of vg and a dominant-negative form of wg. (E) Ectopic expression of vg QE-lacZ (green) in the transformed legs. Notice repression of vg QE-lacZ report (green) in territories with high levels of wg expression (red). (F) Dorsal transformed territories in adult legs are correlated with ap (green) expression. Notice that the annular expression of ap-lacZ in the leg is modified: it is expanded in ventral territories but reduced (white arrowhead) in dorsal ones. The expression of wg (red) is activated at high levels in the border (wing margin) of ap expression. (G) Anterior and posterior specification in transformations denoted by the wild-type expression of en (green). The expression of wg-lacZ (red) corresponding to the wing margin appears in anterior as well as in posterior territories.

View larger version (90K): [in a new window]   Fig. 2. Ectopic wg-vg co-expression driven by vg-G4 causes the transformation of eye territories into wing blade with cuticular structures (A) and gene expression (C,D) characteristic of wing blade. The expression of vg-G4 is detected in the eye imaginal disc by the simultaneous mobilisation of UAS-GFP (GFP) (B-D). Scale bars: 0,1 mm. (A) Observe chaetae (black arrowhead) and wing blade trichomes which appear when we ectopically express vg in the eye. (B) In the wild-type eye imaginal disc, vg-G4 (GFP) and wg (red) are expressed in different territories. High levels of wg expression are detected in the poles of the eye, whereas vg-G4 is expressed in the equatorial line in the eye. (C) Notice the autonomous ectopic expression of nub (red; white arrowhead) in transformed eye cells caused by wg-vg co-expression (GFP). (D) Ectopic expression of vg (red; white arrowhead) in eye transformations caused by the wg-vg co-expression. Notice that the level of wg expression is very low in the transformed territories (white arrowhead).

View larger version (111K): [in a new window]   Fig. 3. Adult phenotypes (A) and imaginal disc gene expression (B-F) caused by the overexpression of vg in clones initiated in the wing blade and wing hinge. Adult clones are labelled with f and delimited by a broken red line. In the imaginal discs, vg clones are associated with green fluorescent protein (GFP). Scale bars: 0.1 mm. (A) Tubular outgrowth including a clone of vg (red arrowhead). The age of clone initiation is 36±12 hours AEL. In the inset a detail of the same clone is shown. (B) In the wing hinge, vg overexpression in clones (green) displaces the rings of wg expression (red) by several cellular diameters. The age of clone initiation is 60±12 hours AEL. (C) In the wing hinge, the vg overexpression in clones (green) non-autonomously activates the expression of Dll (red) and autonomously represses Hth expression (blue). The age of clone initiation is 60±12 hours AEL. (D) In the wing hinge, vg overexpression in clones (green) (white arrowhead) autonomously activates the vg QE-lacZ reporter (red). The age of clone initiation is 60±12 hours AEL. (E) vg overexpression in clones (green; white arrowhead) never activates the vg BE-lacZ reporter (red) reporter in the wing imaginal disc (or in other tissues). The age of clone initiation is 60±12 hours AEL. (F) In all studied tissues, vg overexpression in clones (green; white arrowhead) autonomously activates the sd-lacZ reporter (red). The age of clone initiation is 60±12 hours AEL.

View larger version (103K): [in a new window]   Fig. 4. Adult `mixed' tissue phenotypes (A,B) and imaginal disc expression (C,D) caused by the ectopic clonal expression of vg in the notum. Adult clones are labelled with f and delimited by a broken red line. In the imaginal discs, vg clones are associated with GFP. The age of clone initiation is 36±12 hours AEL. Scale bars: 0.1 mm. (A) Clone of vg ectopic expression in the notum initiated at 36±12 hours AEL; high magnification is shown in B. The clone territory contains trichomes of wing blade (red arrowhead) and notum chaetae in a `salt and pepper' distribution. Notice the differences between trichomes with wing blade characteristics (red arrowhead) contained in the clone with notum trichomes (black arrowhead). (C) Clones of vg ectopic expression (green) in the notum that simultaneously contain cells expressing [dorsal territories (d)] and non-expressing [ventral territories (v)] the ap-lacZ reporter. Notice that endogenous wg expression in the notum appears displaced (yellow arrowhead), whereas wg expression is enhanced within the clone (white arrowhead) at the confrontation between cells expressing and non-expressing ap-lacZ, as occurs in the wild-type wing margin. (D) Adult mixed tissues are correlated, in imaginal discs, with the autonomous expression of wing blade genes such as bs (red). Notice that the expression of bs is non-autonomously induced outside the clone (green; white arrowhead), as well as partially induced within the clone.

View larger version (92K): [in a new window]   Fig. 5. Adult phenotypes (A,B,G) and gene expression patterns caused by the ectopic expression of vg in clones located in the leg (C-F) and eye (H,I) imaginal discs. Adult clones are labelled with f and delimited by a broken red line. In the imaginal discs, vg clones are associated with GFP. Scale bars: 0.1 mm. (A) Clones of vg ectopic expression include `mixed' cuticular differentiation patterns in the leg, with leg chaetae mixed in a `salt and pepper' distribution with wing blade trichomes. In the inset, compare trichomes of the leg (black arrowhead) with wing blade trichomes (red arrowhead). The age of clone initiation is 36±12 hours AEL. (B) Proximalisation phenotypes of the leg without cuticular transformation induced by vg ectopic expression in clones. In distal tarsal segments of the leg, typical chaetes are associated with bracts (black arrowhead in the inset), whereas in vg clones chaeates are not associated with bracts (red arrowhead in the inset). Notice the non-autonomous size reduction in distal tarsal segments of the leg. The age of clone initiation is 36±12 hours AEL. (C) Clones of vg ectopic expression (green) autonomously reduce endogenous wg expression (red; white arrowhead). The age of clone initiation is 60±12 hours AEL. (D) Clones of vg ectopic expression (green) may activate bs (red) expression (white arrowhead) in a subset of cells within the clone. Notice that only those clones situated in ventral leg territories induce bs expression. The age of clone initiation is 60±12 hours AEL. (E,F) Clones of vg ectopic expression (green) in ventral territories of the leg show autonomous expression of the ap-lacZ reporter (red) (E), whereas it is repressed in dorsal territories (F). Notice that ap expression is not detected in all cells of the clone, similar to D. The age of clone initiation is 60±12 hours AEL. (G) Outgrowth with wing blade trichomes (indicated by red arrowhead) induced by vg clone. In the inset, trichomes with wing blade characteristics (red arrowhead) are compared with surrounded ommatidial differentiation (black arrowhead). The age of clone initiation is 36±12 hours AEL. (H) Clones of ectopic vg expression (green) autonomously reduce the expression of wg (red; white arrowhead). The age of clone initiation is 60±12 hours AEL. (I) In the eye, clones of vg ectopic expression (green) autonomously induce the expression of nub (white arrowhead). Only those clones induced in territories with high levels of Wg express nub. The age of clone initiation is 60±12 hours AEL.

View larger version (136K): [in a new window]   Fig. 6. Cuticular phenotypes (A) and imaginal disc expression pattern (B-D) caused by clonal overexpression of wg in the wing imaginal disc. Adult clones are labelled with f and delimited by a broken red line. In the imaginal discs, wg clones are associated with GFP. Scale bars: 0.1 mm. (A) Clones of wg overexpression in the notum show the typical differentiation of this territory. In the inset notice that trichomes are equal inside (red arrowhead) and outside the clone (black arrowhead). The age of clone initiation is 36±12 hours AEL. (B) Clones of wg overexpression (green) in the wing blade autonomously and non-autonomously induce the expression of vg (red), whereas those clones outside the wing blade do not express vg (white arrowhead). The age of clone initiation is 60±12 hours AEL. (C) Clones of wg overexpression (green) in the wing imaginal disc autonomous and non-autonomously induce the expression of nub (red; white arrowhead). Notice that non-autonomous expression of nub is detected only in the closest cells surrounding the clone. The age of clone initiation is 60±12 hours AEL. (D) Clones of wg overexpression (green) show homogenous and high levels of Wg (red). The age of clone initiation is 60±12 hours AEL.

View larger version (125K): [in a new window]   Fig. 7. Adult phenotypes (A-C) and imaginal disc expression patterns (D-G) caused by the co-expression of wg and vg in clones in the wing imaginal disc. Adult clones are labelled with f and delimited by a broken red line. In the imaginal discs, wg-vg clones are associated with GFP. Scale bars: 0.1 mm. (A) wg-vg clones in the wing blade may induce the appearance of tubular outgrowths. Notice the large non-autonomous growth induced by the clone. The age of clone initiation is 60±12 hours AEL. (B) Clones situated near the wing margin do not induce outgrowths. The age of clone initiation is 60±12 hours AEL. (C) In the notum, all the cells of wg-vg clones (delimited by a broken red line) differentiate into wing margin sensory elements and non-autonomously induce cuticular transformation to wing blade (delimited by a broken black line). The age of clone initiation is 36±12 hours AEL. (D) wg-vg clones (GFP) induced anywhere within the imaginal disc activate autonomously and non-autonomously the expression of vg (red; white arrowhead). The age of clone initiation is 60±12 hours AEL. (E) wg-vg (GFP) clones show heterogeneous or low levels of wg expression (red; white arrowheads). The age of clone initiation is 60±12 hours AEL. (F) wg-vg clones (GFP) autonomous and non-autonomously activate the expression of nub (red) anywhere in the imaginal disc. Notice that the non-autonomous expression of nub (red) is detected in cells surrounding the clone at long distances. The age of clone initiation is 60±12 hours AEL. (G) wg-vg clones (GFP) in the wing blade autonomously and non-autonomously repress bs (red; white arrowhead) expression, but in the wing hinge or in the notum, bs is autonomously repressed and non-autonomously induced. The age of clone initiation is 60±12 hours AEL.

View larger version (88K): [in a new window]   Fig. 8. Adult phenotypes (A,B) and imaginal disc expression patterns (C,D) caused by the ectopic clonal co-expression of wg and vg in the leg (A,C) and eye (B,E) imaginal discs. Adult clones are labelled with f and delimited by a broken red line. In the imaginal discs, clones are associated with GFP. Age of clone initiation is 60±12 hours AEL. Scale bars: 0.1 mm. (A) wg-vg clones induce a `mixed' cuticular differentiation pattern in the leg. Notice that in the outgrowth chaetae characteristic of the leg appear mixed with wing blade trichomes in a `salt and pepper' distribution. The inset shows the differences between wing blade trichomes of the clone (red arrowhead) and leg trichomes outside the clone (black arrowhead). (B) In the eye, all cells of the wg-vg clones autonomously differentiate into sensory elements of the wing margin. (C) In the leg, wg-vg clones activate the expression of wing blade genes such as bs (red), only in a subset of cells within the clones (arrowhead). Notice that the expression of bs is not detected in all the clones. (D) In the eye, wg-vg clones (GFP) autonomously activate the expression of nub (red) in all positions.

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