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Towards a model of the organisation of planar polarity and pattern in the Drosophila abdomen

¹ MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK
² Howard Hughes Medical Institute, Columbia University College of Physicians and Surgeons, 701 West 168^th Sreet, New York, NY 10032, USA

View larger version (143K): [in a new window]   Fig. 1. Clones that have partial loss of function for ptc and also lack hh. This clone is marked with pawn (the mutant hairs are small and thin and the bristles are depauperate; a dotted line outlines the clone) and shows reversed polarity within the clone and behind it, and therefore eliminates the hypothesis that ectopic Hh is produced by the clone to drive the reversal. The clone makes dark a5 pigment. In this and subsequent figures anterior is upwards. Red arrows indicate the polarity.

View larger version (52K): [in a new window]   Fig. 2. An abdominal segment and effects of omb– clones. Left-hand panel shows a normal segment with nomenclature for the types of cuticle (Struhl et al., 1997b). Right-hand panel is a memorandum for both vectorial and scalar effects of omb– clones (surrounded by red dashed lines) in different positions in both the A and P compartments. The scalar is shown by the colour of the cuticle and the red arrows show the observed polarity of the hairs (which normally point posteriorly), near and within the clones. We imagine the polarity to be a consequence of the concentration landscape for X. For clarity, the hairs have been removed from part of the A compartment on the right. Compare Fig. 3 and Fig. 7.

View larger version (118K): [in a new window]   Fig. 3. omb in the abdomen. (A) The expression of omb.Gal4, monitored by UAS-lacZ expression. At the front of the ß-gal stripe, the boundary is graded, with staining fading out at about one third of the A compartment. Behind, the stripe ceases about half way into the P compartment. (B) A clone of omb– cells, marked with singed (yellow arrowheads) which affects the bristles: bristles often become separated from the body of the clone and hence they provide only a poor indication of the extent of the clone. The preparation is stained for ptc.lacZ which is upregulated by Hh (Struhl et al., 1997b) both inside and outside the clone. Note the omb– territory forms unpigmented (a6) cuticle at the back of the A compartment and lightly pigmented (a3) cuticle more anteriorly, in place of the normal dusky (a4) cuticle (Fig. 2). Polarity in the clone is reversed. (C) A clone of omb– cells, marked with ß-gal. The clone is associated with a patch of reversed polarity which, here and there, extends both in front and behind the clone (visible in the hairs and indicated by the red arrows pointing upwards). The clone itself lacks the dark a4 pigment which is visible anterior and lateral to the clone. Inset shows detail of hair reversals in front of the clone. (D) A clone of omb– cells, marked with ß-gal. This clone is near the back of the A compartment and contains largely reversed hairs; note the autonomy of the effects of omb– on pigment, and the non-autonomy of its effects on polarity. The white arrowhead indicates a patch of dusky (a4) pigment that is just anterior to the clone. Compare Fig. 4B. (E) A clone overexpressing omb, marked with ß-gal. We see the hairs pointing into the centre of the clone giving reversed polarity behind it. In the middle and at the back of the A compartments, clones of this genotype give abnormal cuticle, with reduced pigmentation (not shown). Compare Fig. 4D.

View larger version (25K): [in a new window]   Fig. 4. Loss and overexpression of omb. The diagrams summarise the model. The blue line traces the actual concentration profile of X, with the brown shading indicating the strength of X production. The slope of X concentration is the vector which defines planar polarity at each point. (A) In the wild type the highest concentration of X and the highest rate of production of X coincide in cells at the back of the A compartment. (B) A clone of omb– cells at the back of the A compartment produces little or no X, and so X spreads into it from the front, forming a reversed gradient and reversed polarity. (C) A clone of omb– cells positioned more anteriorly than the clone in (B), X is produced both in front and behind the clone, creating two peaks and producing a reversed gradient that begins within the clone and extends anteriorly. (D) A clone over-expressing X will make a local peak of X, causing reversal within the back of the clone and behind it.

View larger version (79K): [in a new window]   Fig. 5. The Hh pathway, omb and polarity. (A) A clone that lacks both ptc and omb marked with singed. The clone makes a6 cuticle like ptc– clones, but reverses polarity in the front half of the clone as do omb– clones in this position (see Fig. 2, Fig. 5B) and unlike ptc– clones (Lawrence et al., 1999a). (B) A comparison between ptc– and omb– ptc– clones, they both affect the scalar in the same way, making a6 cuticle; but they have very different effects on polarity. (C) A clone of cells, marked with pawn that overexpresses a form of Ptc that blocks Hh reception but not Hh movement. All the pawn cells with A provenance form pigmented (a3) cuticle. The polarity is largely reversed, even at the back of the clone and in some places, behind it. To the left there is a small clone of P provenance.

View larger version (95K): [in a new window]   Fig. 6. The Wnt pathway and polarity. (A,B) Comparison of embryonic clones that are Pka– as well as being otherwise wild type (A) or homozygous for Df(2L)RF (B). This deficiency removes wg as well as Wnts 4, 6 and 10. Both types of clones make a4 cuticle with some a5 bristles (white arrowheads) (Lawrence et al., 1999a). The polarity of hairs at the back of the clones as well as wild-type hairs behind are reversed to a similar extent in both clones (red arrows). Pka– clones carrying the deficiency survive less often than Pka– controls. (C) A clone of sgg– cells, marked with yellow in the anterior region of the A compartment. Note the cluster of five yellow bristles and that the polarity is reversed behind them. The abdomen carries ptc.lacZ and, as in this case, these clones are usually associated with some sporadic up-regulation of ptc, suggesting that the Hh pathway is ectopically activated, inducing a source of X. (D) A clone of sgg– cells marked with yellow and stubby chaete (stc), situated far anterior in the A compartment (stc causes tufts of hairs to form). The a1 cuticle in this region is apparently transformed to make a3 cuticle with hairs and bristles. Some hairs behind the clone have reversed polarity. (E) A clone of sgg– cells marked with stc in the mid-region of the P compartment. The clone is transformed, making hairs characteristic of p3 cuticle. (F) A clone of cells that are mutant for arm in the tergites. The clone is transformed to form large pleural hairs and cuticle. It tends to sort out, forming a rounded shape (Lawrence et al., 1999b) and the polarity of the front of the clone, and of some wild-type cells anterior to the clone, is reversed.

View larger version (105K): [in a new window]   Fig. 7. omb in the posterior compartment. (A) A clone of omb– cells in the P compartment; the nuclei are marked with lacZ. This clone removes nearly all hairs, apparently transforming the cuticle from p3 to p2 type. (B,C) A large arrow– clone in the P compartment marked with pawn. The abdomen carries omb.Gal4 and UAS.lacZ, and we see that, wherever the cells lack arrow as shown by the pawn marker, the ß-gal staining is reduced (see detail in B). This is true of even a single pawn cell that is separated from the main clone (arrowhead in C). Note in B that some hairs anterior to the clone have reversed polarity (red arrow).

View larger version (28K): [in a new window]   Fig. 8. Working model for patterning the chain of A and P compartments. The P compartments are shown in blue. The model applies to the dorsal epidermis of the abdomen, where Hh induces Wg, but can be generalized to the ventral pleura where Wg is replaced by Dpp, both proteins probably performing the equivalent function. In the first step (at top) Hh is produced in the P compartment and spreads into adjacent A cells, generating a U-shaped gradient. In the A compartment, the concentration of Hh at any point provides a scalar which dictates the type of cuticle formed (a1 to a6). Cells in the anterior and posterior regions of the A compartment respond differently to Hh (Struhl et al., 1997b). In the posterior region, peak levels of Hh induce engrailed, wg and omb expression and specify a6, intermediate levels induce only wg and omb and specify a5 and a4, and low levels or no Hh specify a3. In the anterior region, Hh does not induce engrailed, wg and omb, but high levels induce a1, with a2 being specified by low levels or no Hh. In the P compartment, the scalar is provided by Wg, which is produced by cells at the rear of the A compartment and moves across the AP compartment boundary into the P compartment. Peak levels of Wg induce Omb and thereby specify p3; lower levels or no Wg specify p2 and p1. Planar polarity is controlled by a polarizing morphogen ‘X’, produced largely in posterior A cells by Hh acting through Omb. Wg/Wnt helps X production, apparently to ensure that peak levels are generated in response to Hh. In the model shown X then spreads forward, forming a concentration gradient that extends through the entire compartment and possibly into the P compartment in front. The maximal slope of X at any given position provides a vector which specifies planar polarity. Note the model appears to demand that X cannot spread backwards into the P compartment behind the source. See conclusions for an alternative model.