d. Mol. Biol. (1986) 188, 517-528
An Ecdysterone-responsive Puff Site in Drosophila
Contains a Cluster of Seven Differentially
Regulated Genes
Linda L. Restifo and Gregory M. Guild¢
Department of Biology~G5
University of Pennsylvania
Philadelphia, PA 19104, U.S.A.
(Received 2 July 1985, and in revised form 18 November 1985)
We have determined the molecular organization of an ecdysterone-responsive puff site in
Drosophila melanogaster. The 71E puff site contains a tightly linked cluster of at least seven
genes within a neighborhood of 10 x 103 base-pairs. All the genes are expressed in a tissue-
specific manner in either the larval or the prepupal salivary gland. However, these genes
can be divided into two groups on the basis of their temporal pattern of transcription. Six
of the genes are expressed only in prepupal salivary glands and are arranged as three
divergently transcribed pairs. Nestled within this region is one gene expressed primarily in
late third-instar salivary glands. We conclude that this developmentally complex puff site
contains six members of the ecdysterone-induced "late"-gene set and one member of the
ecdysterone-regulated "intermolt"-gene set. Additional complexity is found at the
transcript level: a heterogeneously sized population of RNA molecules arises fi'om each of
the seven genes.
1. Introduction
The larval and prepupal salivary glands of
Drosophila melanogaster offer a model system for
studying co-ordinated gene expression during
development (for a review, see Ashburner &
Berendes, 1978). Transcriptional activity in the
salivary gland genome can be monitored by
observing changes in puffing patterns of the giant
polytene chromosomes. Cytological observations
have shown that the expression of three dispersed
sets of puffs is altered in response to a
developmentally specific concentration increase of
the steroid molting hormone ecdysterone~: that
occurs shortly before the end of the third, and final,
larval instar. The three sets of ecdysterone-sensitive
loci in salivary glands differ in the time-course of
their response to the hormone and their sensitivity
to hormone concentration.
Following the increase in ecdysterone titer, a
small number of previously active larval
chromosomal puffs regress (Ashburner, 1972a, 1973).
t Author to whom all correspondence should be
addressed.
~:Abbreviations used: eedysterone, 20-hydroxy-
ecdysone; kb, 103 bases or base-pairs; SGS, salivary
gland secretion.
0022-2836/86/080517-12 $03.00/0
These puffs represent the "intermolt" genes, some
of which encode protein components of the salivary
gland "glue" (Muskaviteh & Hogness, 1980;
Crowley et al., 1984; Guild & Shore, 1984). Within
minutes of ecdysterone stimulation, a small number
of puff sites (representing the "early" genes) are
induced and persist for several hours. A large
number of sites (representing the "late" genes)
become puffed several hours following exposure to
the hormone; that is, during the prepupal period,
whose onset is marked by characteristic behavioral
and morphological changes (Bainbridge & Bownes,
1981). By this time, ecdysterone titers are declining
(Handler, 1982).
Experiments using salivary gland organ culture
techniques, in which the ecdysterone-responsive
puffing sequence can be mimicked and manipulated,
have clarified the differences between the responses
of the early and late puff sites to the hormone. In
general, the puffing of early sites requires the
continuous presence of ecdysterone, is independent
of protein synthesis, and varies in amplitude in
direct proportion to hormone concentration. In
contrast, the response of late-gene sites requires
protein synthesis, is essentially all-or-none with
respect to hormone concentration, and can occur
prematurely (for some late sites) if ecdysterone is
removed from the culture medium (Ashburner,
517
© 1986AcademicPress Inc. (London)Ltd.