INTRODUCTION
The adult cuticular structures of Drosophila differentiate at
metamorphosis from segmentally derived single-layered
epithelial invaginations called imaginal discs. Each disc
normally forms a fixed portion of the pattern of cuticular
elements of the corresponding segment, but the develop-
mental fates of individual cells are not irreversibly deter-
mined, and the evidence suggests that the fate of a cell can
be influenced both by its lineage history or compartmental
cell-state (Garcia-Bellido et al., 1973) and by positional
information (Wolpert, 1969).
When complementary imaginal disc fragments are cul-
tured in vivo, one fragment can regenerate the part of the
pattern that was deleted, while the other can only duplicate
the part it normally forms in situ (Schubiger, 1971). Thus
the new partial pattern added to each fragment is identical,
but its extent differs depending on the location of the cut.
This suggested that the new pattern might be specified by
positional information at the cut edge common to both frag-
ments (Bryant, 1971; Postlethwaite and Schneiderman,
1973). The way the new pattern is generated in each disc
fragment involves folding of the cut edge and healing to
restore continuity of the epithelial surface across the wound.
The patterns regenerated in a wide variety of experiments
have been explained by postulating strictly local interac-
tions between the cells brought together in this way (French
et al., 1976; Bryant et al., 1981). According to this model,
positional disparities across the wound stimulate local cell
proliferation, resulting in the interpolation of the missing
intermediate positional values.
Clonal labelling of disc cells at the time these events are
initiated (Girton and Russell, 1980; Abbott et al., 1981),
showed that the new pattern is derived from a very small
1287
Development 117, 1287-1297 (1993)
Printed in Great Britain © The Company of Biologists Limited 1993
When imaginal disc fragments from Drosophila are cul-
tured in adult female hosts, they either duplicate the
part of the pattern specified by the fate map, or regen-
erate to replace the missing part. The new tissue is
added by proliferation of a small number of cells from
the cut edge, brought together when the wound heals to
form a regeneration blastema. Specification of the new
pattern has been explained by assuming interactions
among cells of different positional value in the regener-
ation blastema. In order to identify genes which might
mediate these events, we screened over eight hundred
independently isolated autosomal insertions of an
enhancer-sensitive P-element, for altered lac-z expres-
sion in regenerating discs following cell death induced
by a temperature-sensitive cell-lethal mutation. Two
further screens divided the positive lines into four
groups based on appropriate timing of the lac-z response
in the cell-lethal mutant background and the expected
response to an alternate source of cell death. Expression
in wing disc fragments cultured in vivo was most fre-
quent in the target class defined by the screens. In this
direct test, lac-z expression was found in 23 lines and in
most cases was spatially and temporally correlated with
the formation of the regeneration blastema. Our results
suggest a very substantial transcriptional response
during the early stages of imaginal disc regeneration.
lac-z expression in control imaginal discs, embryos and
adult ovaries of the positive lines was also assayed. The
selected insertions included: a small class expressed only
in discs undergoing regeneration and apparently not at
any other stage, possibly representing genes active
exclusively in regeneration; a larger class expressed in
the embryo or during oogenesis, but not normally in
imaginal discs, as expected for functions recruited from
earlier stages of the developmental program; and finally
a class with spatially patterned expression in normal
discs. This class included several insertions with expres-
sion associated with compartment boundaries, including
one at the decapentaplegic (dpp) , and one at the crumbs
(crb) locus, a growth factor homologue, and an EGF-
repeat gene respectively. Some of the expression pat-
terns observed in cultured disc fragments provide evi-
dence for cell communication in the regeneration
blastema.
Key words: imaginal discs; regeneration; enhancer detection,
Drosophila
SUMMARY
Gene expression during imaginal disc regeneration detected using
enhancer-sensitive P-elements
William J. Brook, Lisa M. Ostafichuk, Jana Piorecky, Mark D. Wilkinson, Daralyn J. Hodgetts and
Michael A. Russell
Department of Genetics, University of Alberta, Edmonton, Alberta, CANADA T6G 2E9