incorrect. The spatial signaling roles of zygotic con- 
trol genes such as hb were examined, by forcing 
them to be expressed in portions of the embryo 
where they are normally inactive. In the case of hb, 
this was achieved by placing the hb gene under the 
control of the hsplO promoter and heat-shocking 
early embryos to drive ubiquitous hb protein ex- 
pression. Surprisingly, ubiquitous hb expression 
caused a phenotype that appears indistinguishable 
from that caused by mutations that block activity of 
the nanos morphogen. This unexpected result fo- 
cused attention on the prior demonstration by Dr. 
Diethard Tautz that the nanos morphogen nor- 
mally blocks expression of hb protein in the poste- 
rior half of the body by destabilizing maternal tran- 
scripts of the gene that are initially distributed 
throughout the fertilized egg. These findings sug- 
gested that the nanos morphogen may normally 
have only a single role-blocking posterior expres- 
sion of hb protein from maternally derived tran- 
scripts. This possibility has been shown to be cor- 
rect by eliminating the maternally derived activities 
of both the hb and nanos gene products. Embryos 
that lack both activities give rise to normal larvae 
and adults. 
The demonstration that early embryos lacking 
the primary posterior determinant system can de- 
velop normal body patterns under some conditions 
leads to the surprising conclusion that the nanos 
morphogen system is not directly responsible for 
organizing posterior body pattern. Instead, it seems 
to play a permissive rather than an instructive role. 
This is in striking contrast to the bed morphogen 
system, which dictates anterior body pattern via its 
multiple direct effects on subordinate signaling 
molecules (e.g., transcription activation of the hb 
gene) and poses the question of what factors are 
responsible for specifying the posterior pattern. 
Preliminary experiments in which the hsplO pro- 
moter is used to drive ubiquitous expression of other 
early control genes, such as Kriippel and knirps, 
suggest that the local distributions of their protein 
products specify posterior body pattern. The mech- 
anisms responsible for ensuring the orderly expres- 
PUBLICATIONS 
sion of these gene products in the absence of any 
single morphogen gradient comparable to the ante- 
rior bed gradient are under investigation. 
III. Terminal System. 
Recent studies of Drs. Trudi Schiipbach, Eric 
Wieshaus, Christiane Niisslein-Volhard, and their 
colleagues have established the existence of a third 
primary determinant system that distinguishes end 
portions of the body pattern from the middle por- 
tion. Moreover, the primary morphogen in this sys- 
tem appears to be encoded by the torso gene, 
which encodes a receptor tyrosine kinase. 
In studies performed in this laboratory, the torso 
protein has been shown to be expressed ubiqui- 
tously on the surface of early embryos, despite ge- 
netic experiments that indicate that it normally acts 
selectively at both poles but must be inactive in the 
middle portion of the body. This finding argues 
strongly that the torso protein functions as a ubiq- 
uitous surface receptor that is activated only in the 
vicinity of the poles. Additional genetic and immu- 
nohistochemical experiments have confirmed this 
conclusion and suggested that the torso protein is 
activated by a localized ligand tethered to the extra- 
cellular matrix surrounding the early embryo. Fi- 
nally, a mutation conferring temperature-sensitive, 
ligand-independent activity of the torso protein has 
been used to show that different levels of activity of 
the protein can specify the development of differ- 
ent portions of the terminal body pattern— pro- 
gressively higher levels specify successively more 
terminal structures. This suggests that localized ac- 
tivity of the torso kinase triggered at both ends of 
the body is translated into opposing gradients of in- 
tracellular signaling molecules— possibly phos- 
phorylated substrates of the kinase— which govern 
the specification of the anterior and posterior ter- 
minalia. 
Dr. Struhl is also Assistant Professor of Genetics 
and Development at the Columbia University Col- 
lege of Physicians and Surgeons. 
Articles 
Macdonald, PM., and Struhl, G. 1988. Cis-acting sequences responsible for anterior localization of bicoid 
mRNA in Drosophila embryos. Nature 336:595-598. 
Struhl, G. 1989. Differing strategies for organizing anterior and posterior body pattern in Drosophila em- 
bryos. Nature 338:741-744. 
Continued 
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