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. 2006 Sep 12;103(37):13734-9.
doi: 10.1073/pnas.0606092103. Epub 2006 Sep 1.

Control of growth and positional information by the graded vestigial expression pattern in the wing of Drosophila melanogaster

L A Baena-Lopez  1 , A García-Bellido
Affiliations

Control of growth and positional information by the graded vestigial expression pattern in the wing of Drosophila melanogaster

L A Baena-Lopez et al. Proc Natl Acad Sci U S A. .

Abstract

The size and shape of organs depend on cellular processes such as cell proliferation, cell survival, and spatial arrangement of cells. In turn, all of these processes are a consequence of positional identity of individual cells in whole organs. Links of positional information with organ growth and pattern expression of genes is a little-addressed question. We show that differences in vestigial expression between neighboring cells of the wing blade autonomously and nonautonomously affect cell proliferation along the proximo-distal axis. On the other hand, uniform expression of vestigial inhibits cell proliferation and also perturbs the shape of wing blade altering the preferential orientation of cell divisions. Our observations provide evidence that local cell interactions, triggered by differences in vestigial expression between neighboring cells, confer positional values operating in the control of growth and shape of the wing.

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Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.
Fig. 1.
vg is heterogeneously expressed in the wing blade. (A) The expression of Vg (yellow) and Wg (blue) are shown in the wing blade (surface view to the left and longitudinal confocal sections to the right) in wing discs of late third instar larvae. (B) Intensity profiles of fluorescence along the P/D (Upper) and A/P (Lower) axes of growth. Yellow and blue lines correspond to vg and wg expression, respectively in B. D/V boundary and vein territories are indicated as D/V and (–5) in A and B.
Fig. 2.
Fig. 2.
The loss of function of vg autonomously and nonautonomously reduces growth in the wing blade in a dose and position manner. (A) Plot summarizing the size distribution of clones defective in Vg expression that simultaneously overexpress the cell death inhibitor puc. Clones are represented as red shadows in A. Notice that the size and frequency of clones diminishes in those territories expressing higher levels of vg (48–72 h AEL). (B) The overexpression of a vg-RNAi driven by dllG4md23 reduces the size of the wing blade along the axes of growth in a dose-dependent manner (increasing reductions with increase of temperature). (C) The overexpression of a vg-RNAi construct driven by enG4 (red wing) reduces the WT size of the wing (blue wing), autonomously (posterior compartment) and nonautonomously (anterior compartment, −13.5%). (D) The overexpression clones of a vg-RNAi construct (green) autonomously diminish the expression of Vg (red) and show an atypical triangular shape (48–72 h AEL) (these clones are narrower when approaching the wing margin). Wg expression (blue) reveals the D/V boundary of the wing and delimits wing blade territories.
Fig. 3.
Fig. 3.
Cell proliferation in the wing blade is maintained in response to heterogeneities of vg expression between neighboring cells. (A) The overexpression of vg under the control of several G4 at 25°C alters the growth and shape of the wing blade. The growth of the wings is strongly reduced in the experimental conditions shown in A. (B) The expression of the reporter proliferating cell nuclear antigen (PCNA) (green) is down-regulated in the wing blade (asterisk) but is up-regulated in the wing hinge (arrows) when vg is overexpressed under the control of ptcG4 (ptcG4 is expressed in a narrow band of anterior cells along the A/P compartment border). Wg expression (red) reveals the D/V boundary of the wing and delimits wing blade territories in B. (C) Size distribution of either WT clones (Left, ●) or vg-expressing clones (Right, ●) and their associated twins (□) in the wing along the P/D axis. The increment of area is represented in y axis of the graphs, whereas the distance of clones and twins to the D/V boundary is shown in the x axis in C. Unlike the WT clones and their twins, the size of vg-expressing clones and their twins is increased when far away from the D/V boundary and also are smaller than controls near the wing margin (red arrowhead). (D) Mitoses (green, PH3) in the WT dllG4md23 domain (purple). (E) Mitoses (green, PH3) in a mutant background dllGmd23/UASvg preferably appear in cells confronting different levels of vg (arrows). dllG4md23 domain is shown in purple.
Fig. 4.
Fig. 4.
The heterogeneous expression of vg in the wing blade modulates the whole length of cell cycle. The cell doubling time (CDT) (hours in the y axis of the graphs) corresponding to either vg-expressing cells and surrounding WT cells (A) or cells defective in vg expression (B). (A) vg-expressing clones and their associated twins in the wing hinge show the CDT shortened compared with controls and also in respect to clones appearing in the wing blade. (B) Loss-of-function clones of vg in the wing blade (cells expressing the vg-RNAi construct) show increased CDT compared with controls.
Fig. 5.
Fig. 5.
The heterogeneous expression of vg favors the orientation of cell division in the wing blade along P/D axis. (A) Clonal growth (green) in a WT background is orientated preferentially along the P/D axis (arrow). (B) Clones (green) in a mutant background overexpressing vg (nubG4K/UASvg) fail to grow preferentially along the P/D axis (arrowheads). Wg expression defines wing blade territories (purple in A and B). (C) Graph summarizing the angle of cell division in respect to the D/V boundary (x axis) in either a WT wing blade (black bars) or in a mutant background (gray bars) overexpressing vg (nubG4K/UASvg). Notice that the orientation of cell division is perturbed in a mutant background overexpressing vg (nubG4K/UASvg) (gray bars) in respect to controls (black bars).
Fig. 6.
Fig. 6.
The expression of Wg is required only to the cell survival of cells expressing vg. Shown are mutant clones for both receptors of Wg (fz1 and Dfz2) that simultaneously overexpress vg (green) (fz1Dfz2-UASvg). (A) The size of fz1Dfz2-UASvg clones in the wing is increased when they appear far away from the D/V boundary 48 h after heat-shock induction. (B) fz1Dfz2-UASvg clones disappear from the wing epithelium 72 h after heat shock. Nuclear GFP is fragmented as a reporter of cell death (arrowhead and B Inset). Nonautonomous effects on growth and patterning of fz1Dfz2-UASvg clones are approximately encircled with orange spots in A and also are indicated with a white arrow in B (notice the outgrowths in the wing discs). Vg and Wg expression are reported in purple in A and B, respectively.
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