Development 110, 105-114 (1990)
Printed in Great Britain © The Company of Biologists Limited 1990
105
The Drosophila segment polarity gene patched is involved in a position-
signalling mechanism in imaginal discs
ROGER G. PHILLIPS
1
, IAN J. H. ROBERTS
1
, PHILIP W. INGHAM
2
and J. ROBERT S. WHITTLE
1
1
School of Biological Sciences, University of Sussex, Brighton, BN1 9QG, UK
2
Molecular Embryology Laboratory, ICRF Developmental Biology Unit, South Parks Road, Oxford, OX1 3PS, UK
Summary
We demonstrate the role of the segment polarity gene
patched (ptc) in patterning in the cuticle of the adult fly.
Genetic mosaics of a lethal allele of patched show that the
contribution of patched varies in a position-specific
manner, defining three regions in the wing where ptc
clones, respectively, behave as wild-type cells, affect vein
formation, or are rarely recovered. Analysis of twin
clones demonstrates that the reduced clone frequency
results from a proliferation failure or cell loss. In the
region where clones upset venation, they autonomously
fail to form veins and also non-autonomously induce
ectopic veins in adjacent wild-type cells. In heteroallelic
combinations with lethal alleles, two viable alleles pro-
duce distinct phenotypes: (1) loss of structures and
mirror-image duplications in the region where patched
clones fail to proliferate; (2) vein abnormalities in the
anterior compartment. We propose that these differ-
ences reflect independently mutable functions within the
gene. We show the pattern of patched transcription in
the developing imaginal wing disc in relation to the
expression of certain other reporter genes using a novel
double-labelling method combining non-radioactive de-
tection of in situ hybridization with /3-galactosidase
detection. The patched transcript is present throughout
the anterior compartment, with a stripe of maximal
intensity along the A/P compartment border extending
into the posterior compartment. We propose that the
patched product is a component of a cell-to-cell position-
signalling mechanism, a proposal consistent with the
predicted structure of the patched protein.
Key words: imaginal discs, pattern formation, cell
communication, segment polarity, patched, Drosophila.
Introduction
The body of the Drosophila adult is derived from a
series of embryonic primordia (imaginal discs) which
undergo extensive rounds of cell division during the
larval stages of development (Auerbach, 1936; Noth-
iger, 1972). Although these cells receive instructions
about their segmental identity during embryogenesis
(Akam, 1987; Peifer et al. 1987), clonal analysis has
shown that their early lineage, with the exception of the
anterior-posterior compartmentalisation event (Gar-
cia-Bellido et al. 1973), is largely indeterminate (Gar-
cia-Bellido and Merriam, 1971; Bryant, 1970). The
information required for the patterning of cells in
different structures is thus an emergent property, which
presumably depends upon communication between
cells as they proliferate. A large body of data shows that
imaginal disc cells respond to changes in the identity of
neighbouring cells whether these alterations are made
by surgical or genetic changes (reviewed in Whittle,
1990). When normally distant parts of a mature wing
disc are juxtaposed and allowed to proliferate, the
intervening pattern of cell types is regenerated by a
process known as intercalation (Haynie and Bryant,
1976). In some genetic mosaics, wild-type cells respond
to neighbours of changed genotype by differentiating
cell types in changed patterns (Stern, 1956; Simpson
and Schneiderman, 1975; Mohler, 1988; Santamaria et
al. 1989) or polarities (Gubb and Garcia-Bellido, 1982;
Vinson and Adler, 1987). In contrast to the early events
of embryonic patterning (Ingham, 1988), virtually
nothing is known about the molecular basis of this
process.
Amongst the many mutations that disrupt adult
morphogenesis are viable alleles of some of the segment
polarity genes, a class originally defined by embryonic
lethal mutations (Niisslein-Volhard and Weischaus,
1980; Niisslein-Volhard et al. 1984). An increasing body
of evidence has implicated these genes in cell interac-
tions (Martinez-Arias et al. 1988; DiNardo et al. 1988;
Mohler, 1988). Here we show that mutations of the
segment polarity gene patched (ptc) disrupt cell pattern-
ing in the cuticle of the adult fly. Using genetic mosaics
of patched we find a requirement for this gene in cells in
specific regions of the wing, which is not rescued by
neighbouring cells; moreover in some locations the
effects of patched mutations extend beyond the limit of
the mosaic, suggesting a role for the gene in a signal