The Drosophila gene atonal encodes a basic helix-loop-helix protein similar to those encoded by the proneural genes of the achaete-scute complex (AS-C). The AS-C are required in the Drosophila PNS for the selection of neural precursors of external sense organs. We have isolated mutants of atonal, which reveal that this gene encodes the proneural gene for chordotonal organs and photoreceptors. In atonal mutants, all observable adult chordotonal organs, and almost all embryonic chordotonal organs fail to form; all adult photoreceptors are missing. For both types of sense organ, this defect is already apparent at the level of precursor formation. Therefore it is a failure in the epidermal-neural decision process i.e. a proneural defect. The failure to form photoreceptors results in atrophy of the atonal mutant imaginal disc, due to apoptosis and lack of stimulation of division. Lack of photoreceptors should also eliminate signalling that arises from differentiating photoreceptors and is required for morphogenetic furrow movement in the wild-type eye disc. Nevertheless, a remnant morphogenetic furrow is still observed in the atonal mutant disc. This presumably reflects the process of furrow initiation, which would not depend on signals from developing photoreceptors.
Reference
Artavanis-Tsakonas
S.
, Simpson
P.
(1991
) Choosing a cell fate: a view from the Notch locus.
Trends Genet
7
, 403
–.Baker
N. E.
, Mlodzik
M.
, Rubin
G. M.
(1990
) Spacing differentiation in the developing Drosophila eye: a fibrinogen-related lateral inhibitor encoded by scabrous.
Science
250
, 1370
–.Baker
N. E.
, Rubin
G. M.
(1992
) Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs.
Dev. Biol
150
, 381
–.Banerjee
U.
, Zipursky
S. L.
(1990
) The role of cell-cell interaction in the development of the Drosophila visual system.
Neuron
4
, 177
–.Basler
K.
, Hafen
E.
(1991
) Specification of cell fate in the developing eye of Drosophila.
BioEssays
13
, 621
–.Bässler
U.
(1973
) Zur Steuerung aktiver Beuregungen des Femur-Tibia-Gelenkes der Stabheuschrecke Carausius morosus.
Kybernetik
13
, 38
–53
Bässler
U.
(1977
) Sensory control of leg movement in the stick insect Carausius morosus.
Biol. Cybernetics
25
, 61
–72
Blackman
R. K.
, Sanicola
M.
, Raftery
L. A.
, Gillevet
T.
, Gelbart
W. M.
(1991
) An extensive 3 cis -regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-family in Drosophila.
Development
111
, 657
–.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
–.Brand
M.
, Jarman
A. P.
, Jan
L. Y.
, Jan
Y. N.
(1993
) asense is a Drosophila neural precursor gene and is capable of initiating sense organ development.
Development
119
, 1
–.Brown
N. L.
, Sattler
C. A.
, Markey
D. R.
, Carroll
S. B.
(1991
) hairy function in the Drosophila eye: normal expression is dispensable but ectopic expression alters cell fates.
Development
113
, 1245
–.Cagan
R. L.
, Ready
D. L.
(1989
) Notch is required for successive decisions in the developing Drosophila retina.
Genes Dev
3
, 1099
–.Campos-Ortega
J. A.
(1988
) Cellular interactions during early neurogenesis in Drosophila melanogaster.
Trends Neurosci
11
, 400
–.Campuzano
S.
, Modolell
J.
(1992
) Patterning of the Drosophila nervous system: the achaete-scute gene complex.
Trends Genet
8
, 202
–.Caudy
M.
, Grell
E. H.
, Dambly-Chaudiere
C.
, Ghysen
A.
, Jan
L.Y.
, Jan
Y.N.
(1988
) The maternal sex determination gene daughterless has a zygotic activity necessary for the formation of peripheral neurons in Drosophila.
Genes Dev
2
, 843
–.Cheyette
B. N. R.
, Green
P. J.
, Martin
K.
, Garren
H.
, Hartenstein
V.
, Zipursky
S. L.
(1994
) The Drosophilasine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system.
Neuron
12
, 977
–.Cubas
P.
, de Celis
J.-F.
, Campuzano
S.
, Modolell
J.
(1991
) Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila wing disc.
Genes Dev
5
, 996
–.Cubas
P.
, Modolell
J.
(1993
) The extramacrochaetae gene provides information for sensory organ patterning.
EMBO J
11
, 3385
–.Dambly-Chaudiere
C.
, Ghysen
A.
(1987
) Independent subpatterns of sense organs require independent genes of the achaete-scute complex in Drosophila larvae.
Genes Dev
1
, 297
–.Ellis
M. C.
, Weber
U.
, Wiersdorff
V.
, Mlodzik
M.
(1994
) Confrontation of scabrous expressing and non-expressing cells is essential for normal ommatidial spacing in the Drosophila eye.
Development
120
, 1959
–.Ghysen
A.
, Dambly-Chaudiere
C.
(1989
) Genesis of the Drosophila peripheral nervous system.
Trends Genet
5
, 251
–.Ghysen
A.
, Dambly-Chaudiere
C.
, Jan
L. Y.
, Jan
Y. N.
(1993
) Cell interactions and gene interactions in peripheral neurogenesis.
Genes Dev
7
, 723
–.Heberlein
U.
, Wolff
T.
, Rubin
G. M.
(1993
) The TGFb homolog dpp and the segment polarity gene hedgehog are required for propagation of a morphogenetic wave in the Drosophila retina.
Cell
75
, 913
–.Jarman
A. P.
, Grau
Y.
, Jan
L. Y.
, Jan
Y. N.
(1993
) atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system.
Cell
73
, 1307
–.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
–.Jimenez
F.
, Campos-Ortega
J. A.
(1987
) Genes in the subdivision 1B of the Drosophila melanogaster X-chromosome and their influence on neural development.
J. Neurogen
4
, 179
–.Jimenez
F.
, Campos-Ortega
J. A.
(1990
) Defective neuroblast commitment in mutants of the achaete-scute complex and adjacent genes of D. melanogaster.
Neuron
5
, 81
–.Ma
C.
, Zhou
Y.
, Beachy
P. A.
, Moses
K.
(1993
) The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye.
Cell
75
, 927
–.Moses
K.
, Ellis
M. C.
, Rubin
G. M.
(1989
) The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells.
Nature
340
, 531
–.Moses
K.
, Rubin
G. M.
(1991
) glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing eye.
Genes Dev
5
, 583
–.Quiring
R.
, Walldorf
U.
, Kloter
U.
, Gehring
W. J.
(1994
) Homology of the eyeless gene of Drosophila to the small eye gene in mice and aniridia in humans.
Science
265
, 785
–.Ready
D. F.
(1989
) A multifaceted approach to neural development.
Trends Neurosci
12
, 102
–.Romani
S.
, Campuzano
S.
, Macagno
E.
, Modolell
J.
(1989
) Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development.
Genes Dev
3
, 997
–.Rubin
G. R.
(1991
) Signal transduction and the fate of the R7 photoreceptor in Drosophila.
Trends Genet
7
, 372
–.Skeath
J. B.
, Carroll
S. B.
(1991
) Regulation of achaete-scute gene expression and sensory organ formation in the Drosophila wing.
Genes Dev
5
, 984
–.Skeath
J. B.
, Panganiban
G.
, Selegue
J.
, Carroll
S. B.
(1992
) Gene regulation in two dimensions: the proneural achaete and scute genes are controlled by combinations of axis-patterning genes through a common intergenic control region.
Genes Dev
6
, 2606
–.Tomlinson
A.
(1985
) The cellular dynamics of pattern formation in the eye of Drosophila.
J. Embryol. Exp. Morphol
89
, 313
–.Thomas
B. J.
, Gunning
D. A.
, Cho
J.
, Zipursky
S. L.
(1994
) Cell cycle progression in the developing Drosophila eye: roughex encodes a novel protein required for the establishment of G1.
Cell
77
, 1003
–.Usherwood
et al. . (1968
) Structure and physiology of a chordotonal organ in the locust leg.
J. Exp. Biol
48
, 305
–323
Van Doren
M.
, Powell
P. A.
, Pasgernak
D.
, Posakony
J. W.
(1992
) Spatial patterning of proneural clusters in the Drosophila wing imaginal disc: auto-and cross-regulation of achaete is antagonized by extramacrochaetae.
Genes Dev
6
, 2592
–.Wolff
T.
, Ready
D. F.
(1991
) Cell death in normal and rough eye mutants of Drosophila.
Development
113
, 825
–.Wolff
T.
, Ready
D. F.
(1991
) The beginning of pattern formation in the Drosophila compound eye: the morphogenetic furrow and the second mitotic wave.
Development
113
, 841
–.Zipursky
S. L.
, Venkatesh
T. R.
, Teplow
D. B.
, Benzer
S.
(1984
) Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes.
Cell
36
, 15
–.
This content is only available via PDF.
© 1995 by Company of Biologists
1995
