Genes of the spalt family encode nuclear zinc finger proteins. In Drosophila melanogaster, they are necessary for the establishment of head/trunk identity, correct tracheal migration and patterning of the wing imaginal disc. Spalt proteins display a predominant pattern of expression in the nervous system, not only in Drosophila but also in species of fish, mouse, frog and human, suggesting an evolutionarily conserved role for these proteins in nervous system development. Here we show that Spalt works as a cell fate switch between two EGFR-induced cell types, the oenocytes and the precursors of the pentascolopodial organ in the embryonic peripheral nervous system. We show that removal of spalt increases the number of scolopodia, as a result of extra secondary recruitment of precursor cells at the expense of the oenocytes. In addition, the absence of spalt causes defects in the normal migration of the pentascolopodial organ. The dual function of spalt in the development of this organ, recruitment of precursors and migration, is reminiscent of its role in tracheal formation and of the role of a spalt homologue, sem-4, in the Caenorhabditis elegans nervous system.
Reference
Anderson
M. G.
, Perkins
G. L.
, Chittick
P.
, Shribley
R. J.
, Johnson
W. A.
(1995
) drifter, a Drosophila POU-domain transcription factor, is required for correct differentiation and migration of tracheal cells and midline glia.
Genes Dev
9
, 123
–137
Barrio
R.
, de Celis
J. F.
, Bolshakov
S.
, Kafatos
F. C.
(1999
) Identification of regulatory regions driving the expression of the Drosophila spalt complex at different developmental stages.
Dev. Biol
215
, 33
–47
Basson
M.
, Horvitz
H. R.
(1996
) The Caenorhabditiselegans gene sem-4 controls neuronal and mesodermal cell development and encodes a zinc finger protein.
Genes Dev
10
, 1953
–65
Bellen
H. J.
, Kooyer
S.
, D'Evelyn
D.
, Pearlman
J.
(1992
) The Drosophila Couch potato protein is expressed in nuclei of peripheral neuronal precursors and shows homology to RNA-binding proteins.
Genes Dev
6
, 2125
–2136
Bier
E.
, Jan
L. Y.
, Yan
Y. N.
(1990
) rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster.
Genes Dev
4
, 190
–203
Blochlinger
K.
, Bodmer
R.
, Jan
L. Y.
, Jan
Y. N.
(1990
) Patterns of expression of Cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos.
Genes Dev
4
, 1322
–31
Brand
A. H.
, Perrimon
N.
(1993
) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
Development,
118
, 401
–415
Brewster
R.
, Bodmer
R.
(1995
) Origin and specification of type II sensory neurons in Drosophila.
Development
121
, 2923
–36
Brewster
R.
, Bodmer
R.
(1996
) Cell lineage analysis of the Drosophila peripheral nervous system.
Dev. Genet
18
, 50
–63
Buck
A.
, Archangelo
L.
, Dixkens
C.
, Kohlhase
J.
(2000
) Molecular cloning, chromosomal localization, and expression of the murine SALL1 ortholog Sall1.
Cytogenet. Cell Genet
89
, 150
–153
Campbell
G.
, Goring
H.
, Lin
T.
, Spana
E.
, Andersson
S.
, Doe
C. Q.
, Tomlinson
A.
(1994
) RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila.
Development
120
, 2957
–66
Carlson
S. D.
, Hilgers
S. L.
, Juang
J. L.
(1997
) Ultrastructure and blood-nerve barrier of chordotonal organs in the Drosophila embryo.
J. Neurocyt
26
, 377
–388
Carlson
S. D.
, Hilgers
S. L.
, Juang
J. L.
(1997
) First developmental signs of the scolopale (glial) cell and neuron comprising the chordotonal organ in the Drosophila embryo.
Glia
19
, 269
–74
Castelli-Gair
J.
, Greig
S.
, Micklem
G.
, Akam
M.
(1994
) Dissecting the temporal requirements for homeotic gene function.
Development
120
, 1983
–95
Chen
C. K.
, Kuhnlein
R. P.
, Eulenberg
K. G.
, Vincent
S.
, Affolter
M.
, Schuh
R.
(1998
) The transcription factors KNIRPS and KNIRPS RELATED control cell migration and branch morphogenesis during Drosophila tracheal development.
Development
125
, 4959
–4968
Chien
C. T.
, Wang
S.
, Rothenberg
M.
, Jan
L. Y.
, Jan
Y. N.
(1998
) Numb-associated kinase interacts with the phosphotyrosine binding domain of Numb and antagonizes the function of Numb in vivo.
Mol. Cell. Biol
18
, 598
–607
de Celis
J. F.
, Barrio
R.
(2000
) Function of the spalt/spalt-related gene complex in positioning the veins in the Drosophila wing.
Mech. Dev
91
, 31
–41
de Celis
J. F.
, Barrio
R.
, Kafatos
F. C.
(1996
) A gene complex acting downstream of dpp in Drosophila wing morphogenesis.
Nature
381
, 421
–424
de Celis
J. F.
, Barrio
R.
, Kafatos
F. C.
(1999
) Regulation of the spalt / spalt-related gene complex and its function during sensory organ development in the Drosophila thorax.
Development
126
, 2653
–2662
Dominguez
M.
, Wasserman
J. D.
, Freeman
M.
(1998
) Multiple functions of the EGFR receptor in Drosophila eye development.
Curr. Biol
8
, 1039
–1048
Freeman
M.
, Klambt
C.
, Goodman
C. S.
, Rubin
G. M.
(1992
) The argos gene encodes a diffusible factor that regulates cell fate decisions in the Drosophila eye.
Cell
69
, 963
–975
Fujita
S. C.
, Zipursky
S. L.
, Benzer
S.
, Ferrus
A.
, Shotwell
S. L.
(1982
) Monoclonal antibodies against the Drosophila nervous system.
Proc. Natl. Acad. Sci. USA
79
, 7929
–33
Gabay
L.
, Seger
R.
, Shilo
B. Z.
(1997
) In situ activation pattern of Drosophila EGFR receptor pathway during development.
Science
277
, 1103
–1106
Gaul
U.
, Mardon
G.
, Rubin
G. M.
(1992
) A putative Ras GTPase activating protein acts as a negative regulator of signaling by the Sevenless receptor tyrosine kinase.
Cell
68
, 1007
–1019
Ghysen
A.
, O'Kane
C.
(1989
) Neural enhancer-like elements as specific cell markers in Drosophila.
Development
105
, 35
–53
Grant
K.
, Hanna-Rose
W.
, Han
M.
(2000
) sem-4 promotes vulval cell-fate determination in Caenorhabditis elegans through regulation of lin-39 Hox.
Dev. Biol
224
, 496
–506
Halter
D. A.
, Urban
J.
, Rickert
C.
, Ner
S. S.
, Ito
K.
, Travers
A. A.
, Technau
G. M.
(1995
) The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophilamelanogaster.
Development
121
, 317
–32
Hartenstein
A. Y.
, Rugendorff
A.
, Tepass
U.
, Hartenstein
V.
(1992
) The function of the neurogenic genes during epithelial development in the Drosophila embryo.
Development,
116
, 1203
–1220
Hartenstein
V.
(1988
) Development of Drosophila larval sensory organs: spatiotemporal pattern of sensory neurons, peripheral axonal pathways and sensilla differentiation.
Development
102
, 869
–886
Hoch
M.
, Broadie
K.
, Jäckle
H.
, Skaer
H.
(1994
) Sequential fates in a single cell are established by the neurogenic cascade in the Malpighian tubules of Drosophila.
Development
120
, 3439
–3450
Hollemann
T.
, Schuh
R.
, Pieler
T.
, Stick
R.
(1996
) Xenopus Xsal-1, a vertebrate homolog of the region specific homeotic gene spalt of Drosophila.
Mech. Dev
55
, 19
–32
Hummel
T.
, Krukkert
K.
, Roos
J.
, Davis
G.
, Klambt
C.
(2000
) Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development.
Neuron
26
, 357
–370
Jarman
A. P.
, Grell
E. H.
, Ackerman
L.
, Jan
L. Y.
, Jan
Y. N.
(1994
) Atonal is the proneural gene for Drosophila photoreceptors.
Nature
369
, 398
–400
Jones
B. W.
, Fetter
R. D.
, Tear
G.
, Goodman
C. S.
(1995
) glial cells missing: a genetic switch that controls glial versus neuronal fate.
Cell
82
, 1013
–1023
Jurgens
G.
(1988
) Head and tail development of the Drosophila embryo involves spalt, a novel homeotic gene.
EMBO J
7
, 189
–196
Kohlhase
J.
, Hausmann
S.
, Stojmenovic
G.
, Dixkens
C.
, Bink
K.
, Schulz-Schaeffer
W.
, Altmann
M.
, Engel
W.
(1999
) SALL3, a new member of the human spalt -like gene family, maps to 18q23.
Genomics
62
, 216
–222
Kohlhase
J.
, Taschner
P. E.
, Burfeind
P.
, Pasche
B.
, Newman
B.
, Blanck
C.
, Breuning
M. H.
, ten Kate
L. P.
, Maaswinkel-Mooy
P.
, Mitulla
B.
, et al. . (1999
) Molecular analysis of SALL1 mutations in Townes-Brocks syndrome.
Am. J. Hum. Genet
64
, 435
–445
Kohlhase
J.
, Wischermann
A.
, Reichenbach
H.
, Froster
U.
, Engel
W.
(1998
) Mutations in the SALL1 putative transcription factor gene cause Townes-Brocks syndrome.
Nat. Genet
18
, 81
–83
Kolodkin
A. L.
, Pickup
A. T.
, Lin
D. M.
, Goodman
C. S.
, Banerjee
U.
(1994
) Characterization of Star and its interactions with sevenless and EGFR receptor during photoreceptor cell development in Drosophila.
Development
120
, 1731
–1745
Köster
R.
, Stick
R.
, Loosli
F.
, Wittbrodt
J.
(1997
) Medaka spalt acts as a target gene of hedgehog signalling.
Development
124
, 3147
–3156
Kramer
S.
, Okabe
M.
, Hacohen
N.
, Krasnow
M. A.
, Hiromi
Y.
(1999
) Sprouty: a common antagonist of FGF and EGFR signaling pathways in Drosophila.
Development
126
, 2515
–2525
Kretzschmar
D.
, Brunner
A.
, Wiersdorff
V.
, Pflugfelder
G. O.
, Heisenberg
M.
, Schneuwly
S.
(1992
) Giant lens, a gene involved in cell determination and axon guidance in the visual system of Drosophila melanogaster.
EMBO J
11
, 2531
–2539
Kuhnlein
R. P.
, Frömmer
G.
, Friedrich
M.
, Gonzalez-Gaitán
M.
, Wever
A.
, Wagner-Bernholz
J. F.
, Gehring
W. J.
, Jäckle
H.
, Schuh
R.
(1994
) spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo.
EMBO J
13
, 168
–179
Kuhnlein
R. P.
, Schuh
R.
(1996
) Dual function of the region-specific homeotic gene spalt during Drosophila tracheal system development.
Development
122
, 2215
–2223
Kurant
E.
, Pai
C. Y.
, Sharf
R.
, Halachmi
N.
, Sun
Y. H.
, Salzberg
A.
(1998
) Dorsotonals/homothorax, the Drosophila homologue of meis1, interacts with Extradenticle in patterning of the embryonic PNS.
Development
125
, 1037
–1048
Lage
P.
, Jan
Y. N.
, Jarman
A. P.
(1997
) Requirement for EGFR receptor signalling in neural recruitment during formation of Drosophila chordotonal sense organ clusters.
Curr. Biol
7
, 166
–175
Lai
Z. C.
, Rubin
G. M.
(1992
) Negative control of photoreceptordevelopment in Drosophila by the product of the yan gene, an ETS domain protein.
Cell
70
, 609
–620
Lecuit
T.
, Brook
W. J.
, Ng
M.
, Calleja
M.
, Sun
H.
, Cohen
S. M.
(1996
) Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing.
Nature
381
, 387
–393
Mlodzik
M.
, Baker
N. E.
, Rubin
G. M.
(1990
) Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila.
Genes Dev
4
, 1848
–1861
Nellen
D.
, Burke
R.
, Struhl
G.
, Basler
K.
(1996
) Direct and long range action of a DPP morphogen gradient.
Cell
85
, 357
–368
O'Neill
E. M.
, Rebay
I.
, Tjian
R.
, Rubin
G. M.
(1994
) The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway.
Cell
78
, 137
–47
Okabe
M.
, Okano
H.
(1997
) Two-step induction of chordotonal organ precursors in Drosophila embryogenesis.
Development
124
, 1045
–53
Okabe
M.
, Sawamoto
K.
, Okano
H.
(1996
) The function of the Drosophilaargos gene product in the development of embryonic chordotonal organs.
Dev. Biol
175
, 37
–49
Okano
H.
, Hayashi
S.
, Tanimura
T.
, Sawamoto
K.
, Yoshikawa
S.
, Watanabe
J.
, Iwasaki
M.
, Hirose
S.
, Mikoshiba
K.
, Montell
C.
(1992
) Regulation of Drosophila neural development by a putative secreted protein.
Differentiation
52
, 1
–11
Ott
T.
, Schutz
G.
(1996
) The mouse homolog of the region-specific homeotic gene spalt of Drosophila is expressed in the developing nervous system and in mesoderm-derived structures.
Mech. Dev
56
, 117
–128
Patel
N. H.
(1994
) Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes.
Methods Cell Biol
44
, 445
–487
Price
J. V.
, Clifford
R. J.
, Schupbach
T.
(1989
) The maternal ventralizing locus torpedo Is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGFR receptor homolog.
Cell
56
, 1085
–1092
Reuter
D.
, Kuhnlein
R. P.
, Frommer
G.
, Barrio
R.
, Kafatos
F. C.
, Jäckle
H.
(1996
) Regulation, function and potential origin of the Drosophila gene spaltadjacent, which encodes a secreted protein expressed in the early embryo.
Chromosoma
104
, 445
–454
Rogge
R. D.
, Karlovich
C. A.
, Banerjee
U.
(1991
) Genetic dissection of a neurodevelopmental pathway: Son of sevenless functions downstream of the Sevenless and EGFR receptor tyrosine kinases.
Cell
64
, 39
–48
Roos
J.
, Hummel
T.
, Ng
N.
, Klambt
C.
, Davis
G. W.
(2000
) Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth.
Neuron
26
, 371
–382
Rutledge
B. J.
, Zhang
K.
, Bier
E.
, Jan
Y. N.
, Perrimon
N.
(1992
) The Drosophila spitz gene encodes a putative EGFR-like growth factor involved in dorsal-ventral axis formation and neurogenesis.
Genes Dev
6
, 1503
–1517
Salzberg
A.
, D'Evelyn
D.
, Schulze
K. L.
, Lee
J. K.
, Strumpf
D.
, Tsai
L.
, Bellen
H. J.
(1994
) Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development.
Neuron
13
, 269
–287
Schejter
E. D.
, Shilo
B. Z.
(1989
) The Drosophila EGFR receptor homolog (DER) gene is allelic to faint little ball, a locus essential for embryonic development.
Cell
56
, 1093
–104
Schweitzer
R.
, Shaharabany
M.
, Seger
R.
, Shilo
B. Z.
(1995
) Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination.
Genes Dev
9
, 1518
–1529
Simon
M. A.
, Bowtell
D. D.
, Dodson
G. S.
, Laverty
T. R.
, Rubin
G. M.
(1991
) Ras1 and a putative guanine nucleoside exchange factor perform crucial steps in signaling by the Sevenless protein tyrosine kinase.
Cell
67
, 701
–716
Sturtevant
M. A.
, Biehs
B.
, Marin
E.
, Bier
E.
(1997
) The spalt gene links the A/P compartment boundary to a linear adult structure in the Drosophila wing.
Development
124
, 21
–32
Sweeney
S. T.
, Broadie
K.
, Keane
J.
, Niemann
H.
, O'Kane
C. J.
(1995
) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects.
Neuron
14
, 341
–351
Xiong
W. C.
, Okano
H.
, Patel
N. H.
, Blendy
J. A.
, Montell
C.
(1994
) repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system.
Genes Dev
8
, 981
–994
This content is only available via PDF.
© 2001 by Company of Biologists
2001
-JournalMeeting.png?versionId=3837)
(update)-InPreprints.png?versionId=3837)
-TechniquesAndResources.png?versionId=3837)
-AndreasProkop.png?versionId=3837)
-GSWorkshop.png?versionId=3837)
