The daughterless (da) gene in Drosophila encodes a broadly expressed transcriptional regulator whose specific functions in the control of sex determination and neurogenesis have been extensively examined. We describe here a third major developmental role for this regulatory gene: follicle formation during oogenesis. A survey of da RNA and protein distribution during oogenesis reveals a multiphasic expression pattern that includes both germline and soma. Whereas the germline expression reflects da's role in progeny sex determination, the somatic ovary expression of da correlates with the gene's role during egg chamber morphogenesis. Severe, but viable, hypomorphic da mutant genotypes exhibit dramatic defects during oogenesis, including aberrantly defined follicles and loss of interfollicular stalks. The follicular defects observed in da mutant ovaries are qualitatively very similar to those described in Notch (N) or Delta (Dl) mutant ovaries. Moreover, in the ovary da- alleles exhibit dominant synergistic interactions with N or Dl mutations. We propose that all three of these genes function in the same regulatory pathway to control follicle formation.

REFERENCES

Artavanis-Tsakonas
S.
,
Simpson
P.
(
1991
)
Choosing a cell fate: a view from the Notch locus.
Trends Genet
7
,
403
408
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
Bender
L. B.
,
Kooh
P. J.
,
Muskavitch
M. A. T.
(
1993
)
Complex function and expression of Delta during Drosophila oogenesis.
Genetics
133
,
967
978
Cline
T. W.
(
1984
)
Autoregulatory functioning of a Drosophila gene product that establishes and maintains the sexually determined state.
Genetics
107
,
231
277
Cline
T. W.
(
1988
)
Evidence that sisterless-a and sisterless-b are two of several discrete ‘numerator elements’ of the X/A sex determination signal in Drosophila that switch between two alternative stable expression states.
Genetics
119
,
829
862
Cline
T. W.
(
1989
)
The affairs of daughterless and the promiscuity of developmental regulators.
Cell
59
,
231
234
Cooley
L.
,
Verheyen
E.
,
Ayers
K.
(
1992
)
chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis.
Cell
69
,
173
184
Cronmiller
C.
,
Cline
T. W.
(
1987
)
The Drosophila sex determination gene daughterless has different functions in the germ line versus the soma.
Cell
48
,
479
487
Cronmiller
C.
,
Cummings
C. A.
(
1993
)
The daughterless gene product in Drosophila is a nuclear protein that is broadly expressed throughout the organism during development.
Mech. Dev
42
,
159
169
Cronmiller
C.
,
Schedl
P.
,
Cline
T. W.
(
1988
)
Molecular characterization of daughterless, a Drosophila sex determination gene with multiple roles in development.
Genes Dev
2
,
1666
1676
Geyer
P. K.
,
Patton
J. S.
,
Rodesch
C.
,
Nagoshi
R. N.
(
1993
)
Genetic and molecular characterization of P element-induced mutations reveal that the Drosophila ovarian tumor gene has maternal activity and a variable null phenotype.
Genetics
133
,
265
278
Goode
S.
,
Wright
D.
,
Mahowald
A. P.
(
1992
)
The neurogenic locus brainiac cooperates with the Drosophila EGF receptor to establish the ovarian follicle and to determine its dorsal-ventral polarity.
Development
116
,
177
192
Keyes
L. N.
,
Cline
T. W.
,
Schedl
P.
(
1992
)
The primary sex determination signal of Drosophila acts at the level of transcription.
Cell
68
,
933
943
King
R. C.
,
Aggarwal
S. K.
,
Aggarwal
U.
(
1968
)
The development of the female Drosophila reproductive system.
J. Morphol
124
,
143
166
Lewis
E. B.
,
Bacher
F.
(
1968
)
Method of feeding ethyl methane sulfonate (EMS) to Drosophila males.
Dros. Inf. Serv
43
,
193
–.
Murre
C.
,
McCaw
P. S.
,
Baltimore
D.
(
1989
)
A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins.
Cell
56
,
777
783
Nöthiger
R.
,
Jonglez
M.
,
Leuthold
M.
,
Meier-Gerschwiler
P.
,
Weber
T.
(
1989
)
Sex determination in the germ line of Drosophila depends on genetic signals and inductive somatic factors.
Development
107
,
505
518
Oliver
B.
,
Perrimon
N.
,
Mahowald
A. P.
(
1988
)
Genetic evidence that the sans fille locus is involved in Drosophila sex determination.
Genetics
120
,
159
171
Oliver
B.
,
Pauli
D.
,
Mahowald
A. P.
(
1990
)
Genetic evidence that the ovo locus is involved in Drosophila germ line sex determination.
Genetics
125
,
535
550
Salz
H. K.
(
1992
)
The genetic analysis of snf: A Drosophila sex determination gene required for activation of Sex-lethal in both the germline and the soma.
Genetics
130
,
547
554
Steinmann-Zwicky
M.
(
1988
)
Sex determination in Drosophila: the X-chromosomal gene liz is required for Sxl activity.
EMBO J
7
,
3889
3898
Steinmann-Zwicky
M.
(
1992
)
How do germ cells choose their sex? Drosophila as a paradigm.
Bioessays
14
,
513
518
Van Doren
M.
,
Ellis
H. M.
,
Posakony
J. W.
(
1991
)
The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes.
Development
113
,
245
255
Xu
T.
,
Rebay
I.
,
Fleming
R. J.
,
Scottgale
T. N.
,
Artavanis-Tsakonas
S.
(
1990
)
The Notch locus and the genetic circuitry involved in early Drosophila neurogenesis.
Genes Dev
4
,
464
475
Xu
T.
,
Caron
L. A.
,
Fehon
R. G.
,
Artavanis-Tsakonas
S.
(
1992
)
The involvement of the Notch locus in Drosophila oogenesis.
Development
115
,
913
922
This content is only available via PDF.