INTRODUCTION
The conserved Hox genes function in laying out the body plan
along the anterior-posterior axis of many, and maybe most,
animal phyla (Carroll, 1995; Slack et al., 1993). All Hox genes
encode a protein that contains the DNA-binding protein
domain, the homeodomain (HD) (McGinnis and Krumlauf,
1992). The activity of the Hox genes were initially identified
in Drosophila by the phenotypes produced by loss-of-function
or gain-of-function alleles. A mutation in a Drosophila Hox
gene results in the transformation of one body part into another
(Lewis, 1978; Kaufman et al., 1990). Ironically, most of the
information on how the HOX proteins work has come from the
analysis of the role of Ultrabithorax (UBX) in gut development
and not their role in the determination of segmental identity
(Capovilla et al., 1994). The reason for this is the lack of
knowledge about what genes are specifically regulated by HOX
proteins during determination of segmental identity, and the
lack of knowledge about what activities are required for deter-
mination of segmental identity (Andrews and Scott, 1992).
In gut development, UBX activity is required in the visceral
mesoderm for the synthesis of Decapentaplegic (DPP)
(Capovilla et al., 1994). Using a change of specificity mutation,
UBX has been shown to act directly as a transcriptional
activator of dpp expression (Capovilla et al., 1994). UBX binds
the dpp regulatory region via the HD. However, UBX alone is
unable to recognize with high affinity the cis-regulatory dpp
sequences. UBX requires the cofactor Extradenticle (EXD)
(Chan et al., 1994). Both EXD and UBX activities are required
for determination of the correct segmental identity of paraseg-
ments 5 and 6 (Peifer and Wieschaus, 1990). EXD interacts
with UBX and other HOX proteins through a hexapeptide
sequence of amino acids found in most HOX products
(Johnson et al., 1995; Chan et al., 1996). This UBX-EXD inter-
5049 Development 124, 5049-5062 (1997)
Printed in Great Britain © The Company of Biologists Limited 1997
DEV5134
Both Proboscipedia (PB) and Sex Combs Reduced (SCR)
activities are required for determination of proboscis
identity. Here we show that simultaneous removal of PB
and SCR activity results in a proboscis-to-antenna trans-
formation. Dominant negative PB molecules inhibit the
activity of SCR indicating that PB and SCR interact in a
multimeric protein complex in determination of proboscis
identity. These data suggest that the expression pattern of
PB and SCR and the ability of PB and SCR to interact in
a multimeric complex control the determination of four
adult structures. The absence of PB and SCR expression
leads to antennal identity; expression of only PB leads to
maxillary palp identity; expression of only SCR leads to
tarsus identity; and expression of both PB and SCR, which
results in the formation of a PB-SCR-containing complex,
leads to proboscis identity.
However, the PB-SCR interaction is not detectable in
vitro and is not detectable genetically in the head region
during embryogenesis, indicating the PB-SCR interac-
tion may be regulated and indirect. This regulation may
also explain why ectopic expression of SCR
Q50K
and SCR
do not result in the expected transformation of the
maxillary palp to an antennae and proboscis, respec-
tively.
Previous analysis of the requirements of SCR activity for
adult pattern formation has shown that ectopic expression of
SCR results in an antenna-to-tarsus transformation, but
removal of SCR activity in a clone of cells does not result in
a tarsus-to-arista transformation. Here we show in five inde-
pendent assays the reason for this apparent contradictory
requirement of SCR activity in tarsus determination. SCR
activity is required cell nonautonomously for tarsus determi-
nation. Specifically, we propose that SCR activity is required
in the mesodermal adepithelial cells of all leg imaginal discs
at late second/early third instar larval stage for the synthesis
of a mesoderm-specific, tarsus-inducing, signaling factor,
which after secretion from the adepithelial cells acts on the
overlaying ectodermal cells determining tarsus identity.
This study characterizes a combinatorial interaction between
two HOX proteins; a mechanism that may have a major role
in patterning the anterior-posterior axis of other animals.
Key words: HOX function, proboscipedia, Sex combs reduced,
induction, pattern formation, Drosophila, limb development
SUMMARY
Genetic characterization of the role of the two HOX proteins, Proboscipedia
and Sex Combs Reduced, in determination of adult antennal, tarsal, maxillary
palp and proboscis identities in Drosophila melanogaster
Anthony Percival-Smith*, Jennifer Weber, Elaine Gilfoyle and Peggy Wilson
Department of Zoology, University of Western Ontario, London, Ontario, Canada, N6A 5B7
*Author for correspondence (e-mail: aperciva@julian.uwo.ca)