INTRODUCTION
The development of Drosophila imaginal discs to a large extent
depends on the genetic interactions that take place at the border
between anterior (A) and posterior (P) cells. These two
populations of cells differ as the selector gene engrailed (en)
is expressed in P cells but not in A cells. The limit between A
and P cells is the compartment border and acts as a source of
positional information (reviewed by Lawrence and Struhl,
1996). En activates the diffusible signal Hedgehog (Hh) in P
cells, which signals to A cells and activates two different
morphogens, Wingless (Wg) and Decapentaplegic (Dpp)
(Basler and Struhl, 1994). Wg and Dpp act as general
organisers of the imaginal discs, inducing growth and
specifying different identities in a concentration-dependent
manner (Zecca et al., 1996; Lecuit and Cohen, 1997). This
model has arisen mainly from studies performed on the wing
and leg discs. These are single discs derived from a cluster of
cells of a unique segment in the embryo (Bate and Martínez-
Arias, 1991).
The genital disc, which gives rise to the terminalia of the
adult fly (internal and external genitalia excluding the gonads
and analia) (Bryant, 1978), is organised in a manner
reminiscent of the leg disc (Gorfinkiel et al., 1999; Estrada and
Sánchez-Herrero, 2001). However, there are several
differences between the genital disc and other imaginal discs
that make it an original experimental model (reviewed by
Sánchez and Guerrero, 2001). For example, it is the only
imaginal disc that shows clear sexual dimorphism. The genital
disc is a compound disc formed by the fusion of three different
primordia derived from the embryonic abdominal segments 8,
9 and 10-11 (Nöthiger et al., 1977; Schüpbach et al., 1978;
Dübendorfer and Nöthiger, 1982; Epper and Nöthiger, 1982).
Thus, a genital disc contains a female genital primordium
(derived from segment A8), a male genital primordium
(derived from segment A9) and an anal primordium (derived
from segments A10-11). In females, the female primordium
gives rise to almost all the internal and external genitalia.
The male primordium was considered to be a ‘repressed
primordium’ because its growth is limited and it does not form
any adult structures (Epper and Nöthiger, 1982). However, it
has recently been shown that the male primordium in the
female genital disc gives rise to the parovaria (internal
accessory female glands) (Keisman et al., 2001). The anal
primordium in females gives rise to the female analia. The
converse is true for males. In male genital discs, the male
genital primordium gives rise to the majority of the internal
and external male genital structures. The female genital
295 Development 130, 295-305
© 2003 The Company of Biologists Ltd
doi:10.1242/dev.00214
In both sexes, the Drosophila genital disc comprises three
segmental primordia: the female genital primordium
derived from segment A8, the male genital primordium
derived from segment A9 and the anal primordium derived
from segments A10-11. Each segmental primordium has an
anterior (A) and a posterior (P) compartment, the P cells
of the three segments being contiguous at the lateral edges
of the disc. We show that Hedgehog (Hh) expressed in the
P compartment differentially signals A cells at the AP
compartment border and A cells at the segmental border.
As in the wing imaginal disc, cell lineage restriction of the
AP compartment border is defined by Hh signalling. There
is also a lineage restriction barrier at the segmental
borders, even though the P compartment cells of the three
segments converge in the lateral areas of the disc. Lineage
restriction between segments A9 and A10-11 depends on
factors other than the Hh, En and Hox genes. The
segmental borders, however, can be permeable to some
morphogenetic signals. Furthermore, cell ablation
experiments show that the presence of all primordia (either
the anal or the genital primordium) during development
are required for normal development of genital disc.
Collectively, these findings suggest that interaction between
segmental primordia is required for the normal
development of the genital disc.
Key words: Drosophila genital disc patterning, Hh signalling, Dpp
signalling, Wg signalling, Segmental boundaries, Cell lineage
restriction
SUMMARY
Development of the Drosophila genital disc requires interactions between its
segmental primordia
Nicole Gorfinkiel
1
, Lucas Sánchez
2
and Isabel Guerrero
1,
*
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
*Author for correspondence (e-mail: iguerrero@cbm.uam.es)
Accepted 18 October 2002