Localized expression of the Drosophila rhomboid (rho) gene has been proposed to hyperactivate EGF-Receptor signaling in specific cells during development of the embryo and adult. In this report we use a novel transposon based genetic method, enhancer piracy, to drive ectopic expression of a rho cDNA transgene by endogenous genomic enhancers. Many enhancer piracy transposon-rho insertions cause dominant phenotypes, over half of which cannot be duplicated by ubiquitous expression of rho. Genetic interactions between various dominant enhancer piracy alleles and mutations in the EGF-R/RAS signaling pathway indicate that many of these novel phenotypes result from ectopic activation of EGF-R signaling. Patterned mis-expression of the rho cDNA transgene correlates in several cases with localized dominant enhancer piracy phenotypes. Enhancer piracy lines reveal an unanticipated role for rho in imaginal disc formation and provide the first evidence that mis-expression of rho is sufficient for converting entire intervein sectors into veins. Enhancer piracy may prove to be a general strategy for obtaining dominant alleles of a gene of interest in diverse insects, worms, plants, and potentially in vertebrates such as mice and fish.

REFERENCES

Abad
P.
,
Quiles
C.
,
Tares
S.
,
Piotte
C.
,
Castagnoe-Sereno
P.
,
Abadon
M.
,
Dalmasso
A.
(
1991
)
Sequences homologous to Tc(s) transposable elements of Caenorhabitidis elegans are widely distributed in the phylum Nematoda.
J. Mol. Evol
33
,
251
258
Alberga
A.
,
Boulay
J.-L.
,
Kempe
E.
,
Dennefeld
C.
,
Haenlin
M.
(
1991
)
The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers.
Development
111
,
983
992
Ashburner
M.
,
Thompson
P.
,
Roote
J.
,
Lasko
P. F.
,
Grau
Y.
,
El Messal
M.
,
Roth
S.
,
Simpson
P.
(
1990
)
The genetics of a small autosomal region of Drosophila melanogaster containing the structural gene for alcohol dehydrogenase. VII. Characterization of the region around the snail and cactus loci.
Genetics
126
,
679
694
Bancroft
I.
,
Dean
C.
(
1993
)
Transposition patter of the maize element Ds in Arabidopsis thaliana.
Genetics
134
,
1221
1229
Bang
A. G.
,
Posakony
J. W.
(
1992
)
The Drosophila gene Hairless encodes a novel basic protein that controls alternative cell fates in adult sensory organ development.
Genes Dev
6
,
1752
1769
Bayer
T. A.
,
Campos-Ortega
J.
(
1992
)
A transgene containing lacZ is expressed in primary sensory neurons in zebrafish.
Development
115
,
421
426
Bellen
H. J.
,
O'Kane
C. J.
,
Wilson
C.
,
Grossniklaus
U.
,
Pearson
R. K.
,
Gehring
W. J.
(
1989
)
P-element-mediated enhancer detection: a versatile method to study development in Drosophila.
Genes Dev
3
,
1288
1300
Bier
E.
,
Vaessin
H.
,
Shepherd
S.
,
Lee
K.
,
McCall
K.
,
Barbel
S.
,
Ackerman
L.
,
Carretto
R.
,
Uemura
T.
,
Grell
E.
,
Jan
L. Y.
,
Jan
Y. N.
(
1989
)
Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector.
Genes Dev
3
,
1273
1287
Bier
E.
,
Jan
L. Y.
,
Jan
Y. N.
(
1990
)
rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster.
Genes Dev
4
,
190
203
Brand
A. H.
,
Perrimon
N.
(
1993
)
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
Development
118
,
401
415
Clifford
R. J.
,
Schupbach
T.
(
1992
)
The torpedo (DER) receptor tyrosine kinase is required at multiple times during Drosophila embryogenesis.
Development
115
,
853
872
Freeman
M.
,
Kimmel
B. E.
,
Rubin
G. M.
(
1992
)
Identifying targets of the rough homeobox gene of Drosophila: evidence that rhomboid functions in eye development.
Development
116
,
335
346
Gotwals
P.
,
Fristrom
J. W.
(
1991
)
Three neighboring genes interact with the Broad -complex and the Stubble-stubbleoid locus to affect imaginal disc morphogenesis in Drosophila.
Genetics
127
,
747
759
Grevelding
C.
,
Becker
D.
,
Kunze
R.
,
von Menges
A.
,
Fantes
V.
,
Schell
J.
,
Masterson
R.
(
1992
)
High rates of Ac/Ds germinal transposition in Arabidopsis suitable for gene isolation by insertional mutatgenesis.
Proc. Nat. Acad. Sci
89
,
6085
6089
Klämbt
C.
(
1993
)
The Drosophila gene pointed encodes two ETS-like proteins which are involved in the development of the midline glial cells.
Development
117
,
163
176
Korn
R.
,
Schoor
M.
,
Neuhaus
H.
,
Henseling
U.
,
Soininen
R.
,
Zachgo
J.
,
Gossler
A.
(
1992
)
Enhancer trap integrations in mouse embryonic stem cells give rise to staining patterns in chimeric embryos with a high frequency and detect endogenous genes.
Mech Dev
39
,
95
109
Mayer
U.
,
Nusslein-Volhard
C.
(
1988
)
A group of genes required for pattern formation in the ventral ectoderm of the Drosophila embryo.
Genes Dev
2
,
1496
1511
Raz
E.
,
Shilo
B. Z.
(
1992
)
Dissection of the faint little ball (FLB) phenotype—determination of the development of the Drosophila central nervous system by early interactions in the Ectoderm.
Development
114
,
113
123
Raz
E.
,
Shilo
B. Z.
(
1993
)
Establishment of ventral cell fates in the Drosophila ectoderm requires DER, the EGF receptor homolog.
Genes Dev
7
,
1937
1948
Robertson
H. M.
(
1993
)
The mariner transposable element is widespread in insects.
Nature
362
,
241
245
Ruohola-Baker
H.
,
Grell
E.
,
Chou
T. B.
,
Baker
D.
,
Jan
L. Y.
,
Jan
Y. N.
(
1993
)
Spatially localized rhomboid is required for establishment of the dorsal-ventral axis in Drosophila oogenesis.
Cell
73
,
953
965
Rutledge
B.
,
Zhang
K.
,
Bier
E.
,
Jan
Y. N.
,
Perrimon
N.
(
1992
)
The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis.
Genes Dev
6
,
1503
1517
Schneuwly
S.
,
Klemenz
R.
,
Gehring
W.
(
1987
)
Molecular analysis of the dominant homeotic Antennapedia phenotype.
EMBOJ
6
,
201
206
Scholz
H.
,
Deatrick
J.
,
Klaes
A.
,
Klampt
C.
(
1993
)
Genetic dissection of pointed, a Drosophila gene encoding two ETS-related proteins.
Genetics
135
,
455
468
Schweisguth
F.
,
Posakony
J. W.
(
1994
)
Antagonistic activities of Suppressor of Hairless and hairless control alternative cell fates in the Drosophila adult epidermis.
Development
120
,
1433
1441
Speicher
S. A.
,
Thomas
U.
,
Hinz
U.
,
Knust
E.
(
1994
)
The Serrate locus of Drosophila and its role in morphogenesis of the wing imaginal discs: control of cell proliferation.
Development
120
,
535
544
Sturtevant
M. A.
,
Roark
M.
,
Bier
E.
(
1993
)
The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway.
Genes Dev
7
,
961
973
Tautz
D.
,
Pfeiffle
C.
(
1989
)
A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila reveals translational control of the segmentation gene hunchback.
Chromosoma
98
,
81
85
Topping
J. F.
,
Wei
W.
,
Lindsey
K.
(
1991
)
Functional tagging of regulatory elements in the plant genome.
Development
112
,
1009
1019
Tsay
Y.-F.
,
Frank
M. J.
,
Page
T.
,
Dean
C.
,
Crawford
N. M.
(
1993
)
Identification of a mobile endogenous transposon in Arabidopsis thaliana.
Science
260
,
342
344
Van Vactor
D. L.
,
Cagan
R. L.
,
Kramer
H.
,
Zipursky
S. L.
(
1991
)
Induction in the developing compound eye of Drosophila: multiple mechanisms restrict R7 induction to a single retinal precursor cell.
Cell
67
,
1145
1155
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