In Drosophila as well as many vertebrate systems, germ cells form extraembryonically and migrate into the embryo before navigating toward gonadal mesodermal cells. How the gonadal mesoderm attracts migratory germ cells is not understood in any system. We have taken a genetic approach to identify genes required for germ cell migration in Drosophila. Here we describe the role of zfh-1 in germ cell migration to the gonadal mesoderm. In zfh-1 mutant embryos, the initial association of germ cells and gonadal mesoderm is blocked. Loss of zfh-1 activity disrupts the development of two distinct mesodermal populations: the caudal visceral mesoderm and the gonadal mesoderm. We demonstrate that the caudal visceral mesoderm facilitates the migration of germ cells from the endoderm to the mesoderm. Zfh-1 is also expressed in the gonadal mesoderm throughout the development of this tissue. Ectopic expression of Zfh-1 is sufficient to induce additional gonadal mesodermal cells and to alter the temporal course of gene expression within these cells. Finally, through analysis of a tinman zfh-1 double mutant, we show that zfh-1 acts in conjunction with tinman, another homeodomain protein, in the specification of lateral mesodermal derivatives, including the gonadal mesoderm.

REFERENCES

Azpiazu
N.
,
Frasch
M.
(
1993
)
tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila.
Genes Dev
7
,
1325
1340
Bodmer
R.
(
1993
)
The gene tinman is required for specification of the heart and visceral muscles in Drosophila.
Development
118
,
719
729
Bonini
N. M.
,
Leiserson
W. M.
,
Benzer
S.
(
1993
)
The eyes absent gene: genetic control of cell survival and differentiation in the developing Drosophila eye.
Cell
72
,
379
95
Boyle
M.
,
Bonini
N.
,
DiNardo
S.
(
1997
)
Expression and function of clift in the development of somatic gonadal precursors within the Drosophila mesoderm.
Development
124
,
971
982
Boyle
M.
,
DiNardo
S.
(
1995
)
Specification, migration, and assembly of the somatic cells of the Drosophila gonad.
Development
121
,
1815
1825
Brookman
J.
,
Toosy
A.
,
Shashidhara
L.
,
White
R.
(
1992
)
The 412 retrotransposon and the development of gonadal mesoderm in Drosophila.
Development
116
,
1185
1192
Callaini
G.
,
Riparbelli
M. G.
,
Dallai
R.
(
1995
)
Pole cell migration through the gut wall of the Drosophila embryo: analysis of cell interactions.
Dev. Biol
170
,
365
375
Chou
T. B.
,
Perrimon
N.
(
1992
)
Use of a Yeast Site-Specific Recombinase to Produce Female Germline Chimeras in Drosophila.
Genetics
131
,
643
653
Cumberledge
S.
,
Szabad
J.
,
Sakonju
S.
(
1992
)
Gonad formation and development requires the abd-A domain of the bithorax complex in Drosophila melanogaster.
Development
115
,
395
402
Eldon
E. D.
,
Pirrotta
V.
(
1991
)
Interactions of the Drosophila gap gene giant with maternal and zygotic pattern forming genes.
Development
111
,
367
378
Ephrussi
A.
,
Dickinson
L. K.
,
Lehmann
R.
(
1991
)
oskar organizes the germ plasm and directs localization of the posterior determinant nanos.
Cell
66
,
37
50
Fortini
M. E.
,
Lai
Z.-C.
,
Rubin
G. M.
(
1991
)
The Drosophila zfh-1 and zfh-2 genes encode novel proteins containing both zinc-finger and homeodomain motifs.
Mech. Dev
34
,
113
122
Frasch
M.
(
1995
)
Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo.
Nature
374
,
464
467
Gavis
E. R.
,
Lehmann
R.
(
1992
)
Localization of nanos RNA controls embryonic polarity.
Cell
71
,
301
313
Godin
I.
,
Wylie
C. C.
,
Heasman
J.
(
1990
)
Genital ridges exert long-range effects on mouse primordial germ cell numbers and direction of migration in culture.
Development
108
,
357
363
Gomperts
M.
,
Garcia-Castro
M.
,
Wylie
C.
,
Heasman
J.
(
1994
)
Interactions between primordial germ cells play a role in their migration in mouse embryos.
Development
120
,
135
141
Greig
S.
,
Akam
M.
(
1995
)
The role of homeotic genes in the specification of the Drosophila gonad.
Curr. Biol
5
,
1057
1062
Häcker
U.
,
Kaufmann
E.
,
Hartmann
C.
,
Jurgens
G.
,
Knochel
W.
,
Jäckle
H.
(
1995
)
The Drosophila fork head domain protein crocodile is required for the establishment of head structures.
EMBO J
14
,
5306
5317
Jaglarz
M. K.
,
Howard
K. R.
(
1994
)
Primordial germ cell migration in Drosophila melanogaster is controlled by somatic tissue.
Development
120
,
83
89
Jaglarz
M. K.
,
Howard
K. R.
(
1995
)
The active migration of Drosophila primordial germ cells.
Development
121
,
3495
3504
Lai
Z.-C.
,
Fortini
M. E.
,
Rubin
G. M.
(
1991
)
The embryonic expression patterns of zfh-1 and zfh-2, two Drosophila genes encoding novel zinc-finger homeodomain proteins.
Mech. Dev
34
,
123
134
Lehmann
R.
,
Tautz
D.
(
1994
)
In Situ Hybridization to RNA.
Methods in Cell Biology
44
,
575
598
Lewis
E. B.
(
1978
)
A gene complex controlling segmentation in Drosophila.
Nature
276
,
565
570
Patel
N.
(
1994
)
Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes.
Methods in Cell Biology
44
,
445
487
Rehorn
K. P.
,
Thelen
H.
,
Michelson
A. M.
,
Reuter
R.
(
1996
)
A molecular aspect of hematopoiesis and endoderm development common to vertebrates and Drosophila.
Development
122
,
4023
4031
Riechmann
V.
,
Irion
U.
,
Wilson
R.
,
Grosskortenhaus
R.
,
Leptin
M.
(
1997
)
Control of cell fates and segmentation in the Drosophila mesoderm.
Development
124
,
2915
2922
Samakovlis
C.
,
Hacohen
N.
,
Manning
G.
,
Sutherland
D. C.
,
Guillemin
K.
,
Krasnow
M.
(
1996
)
Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events.
Development
122
,
1395
1407
Singer
J. B.
,
Harbecke
R.
,
Kusch
T.
,
Reuter
R.
,
Lengyel
J. A.
(
1996
)
Drosophila brachyenteron regulates gene activity and morphogenesis in the gut.
Development
12
,
3707
18
Staehling-Hampton
K.
,
Hoffmann
F. M.
,
Baylies
M. K.
,
Rushton
E.
,
Bate
M.
(
1994
)
dpp induces mesodermal gene expression in Drosophila.
Nature
372
,
783
786
Thummel
C. S.
,
Boulet
A. M.
,
Lipshitz
H. D.
(
1988
)
Vectors for Drosophila P element-mediated transformation and tissue culture transfection.
Gene
74
,
445
456
Van Vactor
D.
,
Sink
H.
,
Fambrough
D.
,
Tsoo
R.
,
Goodman
C. S.
(
1993
)
Genes that control neuromuscular specificity in Drosophila.
Cell
73
,
1155
1164
Warrior
R.
(
1994
)
Primordial germ cell migration and the assembly of the Drosophila embryonic gonad.
Dev. Biol
166
,
180
194
Williamson
A.
,
Lehmann
R.
(
1996
)
Germ cell development in Drosophila.
Annu. Rev. Cell Dev. Biol
12
,
365
91
Xu
T.
,
Rubin
G. M.
(
1993
)
Analysis of genetic mosaics in developing and adult Drosophila tissues.
Development
117
,
1223
1237
Zhang
N.
,
Zhang
J.
,
Cheng
Y.
,
Howard
K.
(
1996
)
Identification and genetic analysis of wunen, a gene guiding Drosophila melanogaster germ cell migration.
Genetics
143
,
1231
1241
Zhang
N.
,
Zhang
J.
,
Purcell
K. J.
,
Cheng
Y.
,
Howard
K.
(
1997
)
The Drosophila protein Wunen repels migrating germ cells.
Nature
385
,
64
67
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