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Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disk

Division of Biology and Medicine, MCB Department, Box G-J, Brown University, Providence, RI 02912, USA

View larger version (77K): [in a new window]   Fig. 1. Wing phenotypes of gbb. (A) A wild-type wing. The five longitudinal veins L1-L5 are indicated, as well as the two crossveins, the anterior crossvein (acv) and posterior crossvein (pcv). The A/P compartment boundary is indicated with a broken line. (B) A gbb1/gbb4 wing illustrating a moderate gbb phenotype. The PCV is absent as well as the distal tips of L4 and L5 (arrows). (C) A gbb3/gbb4 wing showing the most severe phenotype produced by the gbb hypomorphic alleles. The PCV is absent, L5 is truncated almost to the base and L4 is truncated distally (arrow). Note that in both B and C, the overall wing size is reduced compared with the wild-type wing in A.

View larger version (315K): [in a new window]   Fig. 2. Phenotypes associated with gbb clones in the posterior compartment. In all cases, the boundaries of the dorsal-ventral overlap of the clone are shown with broken lines. (A) A large gbb null clone in the posterior compartment shows loss of the PCV and the distal tip of L5, as seen in the gbb hypomorphs, but not the distal tip of L4. (B) A gbb null clone including half of the PCV and the L4/PCV junction. The PCV terminates within two to three cells inside of the clone boundary. (C) A gbb null clone mutant for the posterior half of the PCV and including the L5/PCV junction. In this case the PCV terminates two to three cells outside of the clone boundary. Note also that the proximal region of L5 is mutant and is truncated before reaching the margin, even though the tissue more distally is wild type for gbb function. (D) A gbb null clone that does not include the junctions between the PCV and L4 or L5. Although a significant part of the vein is mutant for gbb, the PCV is not interrupted. (E) Loss of gbb only affects the distal quarter of L5 even if more of the vein is covered in the clone (arrow, compare with Fig. 2A). In clones that cross L5 within this distal quarter (F), L5 is truncated at the clone boundary (arrow). (G) Clones that cover proximal L5 up to within the distal quarter truncate the vein as if all of L5 were mutant (vertical arrow), even if the distal most part of the wing is wild type for gbb. Note that this clone also truncates the PCV (horizontal arrow), but in this case, the vein terminates just outside the clone boundary.

View larger version (141K): [in a new window]   Fig. 3. Phenotypes associated with gbb clones in the anterior compartment. In all cases, the boundaries of the double-sided region of the clone are shown with broken lines. (A) A null gbb clone encompassing the entire anterior compartment. The wing is reduced in size and lacks all of distal L5. (B) Another null gbb clone encompassing the entire anterior compartment where L5 extends to the junction with the PCV (arrow). (C,D) Comparisons between wings bearing large anterior gbb clones (at left) and the wild type opposing wing from the same fly (at right). (C) Control wings with a sha marked clone encompassing the entire anterior compartment. The ratio of left:right (L:R) wing in this case is 0.98. (D) gbb mutant anterior clones result in a dramatic reduction in overall wing size. The ratio of L:R is 0.70.

View larger version (122K): [in a new window]   Fig. 4. Fine mapping of the gbb focus in the anterior compartment. Dark field photomicrographs of wings bearing double-sided gbb null clones (dark patches). Clones falling between the anterior margin (L1) and L3 (A,B) have no effect on L5 or overall wing size. Similarly, clones entirely contained within L3 and L4 are wild type (E). Effects on wing size and L5 specification are observed in clones that occupy the entire anterior compartment (C) or all of the region between the L2/L3 intervein and L4 (D).

View larger version (167K): [in a new window]   Fig. 5. Phenotypes associated with local and long-range requirements of dpp. (A) A dpps11/dpps4 wing illustrating a typical shortvein phenotype. In this case, the distal ends of L2, L4 and L5 are truncated. These phenotypes are correlated with local vein promotion requirements for dpp. (B) A dppd5/dpphr56 wing showing a weak disk phenotype. Defects include failure to specify L3 and L4, as well as loss of the intervein between L4 and L5. This phenotype is very similar to that associated with clones of the dpp target gene sal (deCelis et al., 1996). (C) A dpp null clone showing the local effect on promotion of the PCV (compare with Fig. 2B). In this case, the PCV terminates precisely on the clone boundary (horizontal arrow). dpp has a more pronounced effect than gbb on L4, in this case truncating the vein back to the site of the PCV (vertical arrow). (D) A dpp null clone showing effects on the posterior PCV as well as L5. Again, dpp shows a local effect on the PCV but has a more pronounced effect on L5 than gbb (arrows).

View larger version (123K): [in a new window]   Fig. 6. dpp duplications rescue gbb lethality and phenotypes associated with gbb null clones. (A,B) Graphs showing rescue of gbb1/gbb4 transheterozygotes (A) and gbb1/gbb1' homozygotes (B) to adulthood (black bars) and to pupal/pharate stage (hatched bars). dpp duplications cannot rescue gbb null larvae to adulthood, but there is a dramatic rescue of larval lethality to pupal/pharate lethality (B). (C-E) Phenotypes associated with clones both mutant for gbb and carrying four copies of dpp. (C) A large posterior clone. Despite the rescue of gbb lethality and small disk phenotypes, additional doses of dpp fail to rescue PCV loss (arrow), even in clones confined to the posterior compartment. (D) High magnification of the wing in C showing the distal tip of L5. A gbb null clone covering this same region would show loss of the distal quarter of L5 (arrow, compare with Fig. 2G), but with four copies of dpp, the vein is rescued to the margin. Anterior clones mutant for gbb and carrying four copies of the dpp gene (E) show rescue of both wing size and loss of L5 (arrow).

View larger version (92K): [in a new window]   Fig. 7. Phenotypes associated with sax null clones. (A) A large sax null clone occupying most of the posterior compartment. Unlike gbb clones, this clone is not associated with loss of L4, L5 or the PCV. (B) In this wing, two independent clones encompass most of the posterior compartment and half of the anterior compartment. Note that the clone boundary running along the middle of the anterior compartment is associated with an ectopic vein. (C) A large sax null clone occupying the entire anterior compartment. Like the posterior clone in A there is no effect on venation; however, the wing is reduced in size as has been shown previously (Singer et al., 1997).