journal article
Apr 01, 1996
Determination of wing cell fate by the escargot and snail genes in Drosophila
Abstract
ABSTRACT
Insect appendages such as the wing and the leg are formed in response to inductive signals in the embryonic field. In Drosophila, cells receiving such signals initiate developmental programs which allow them to become imaginal discs. Subsequently, these discs autonomously organize patterns specific for each appendage. We here report that two related transcription factors, Escargot and Snail that are expressed in the embryonic wing disc, function as intrinsic determinants of the wing cell fate. In escargot or snail mutant embryos, wing-specific expression of Snail, Vestigial and β-galactosidase regulated by escargot enhancer were found as well as in wild-type embryos. However, in escargot snail double mutant embryos, wing development proceeded until stage 13, but the marker expression was not maintained in later stages, and the invagination of the primordium was absent. From such analyses, it was concluded that Escargot and Snail expression in the wing disc are maintained by their auto- and crossactivation. Ubiquitous escargot or snail expression induced from the hsp70 promoter rescued the escargot snail double mutant phenotype with the effects confined to the prospective wing cells. Similar DNA binding specificities of Escargot and Snail suggest that they control the same set of genes required for wing development. We thus propose the following scenario for early wing disc development. Prospective wing cells respond to the induction by turning on escargot and snail transcription, and become competent for regulation by Escargot and Snail. Such cells initiate auto- and crossregulatory circuits of escargot and snail. The sustained Escargot and Snail expression then activates vestigial and other target genes that are essential for wing development. This maintains the commitment to the wing cell fate and induces wing-specific cell shape change.
Insect appendages such as the wing and the leg are formed in response to inductive signals in the embryonic field. In Drosophila, cells receiving such signals initiate developmental programs which allow them to become imaginal discs. Subsequently, these discs autonomously organize patterns specific for each appendage. We here report that two related transcription factors, Escargot and Snail that are expressed in the embryonic wing disc, function as intrinsic determinants of the wing cell fate. In escargot or snail mutant embryos, wing-specific expression of Snail, Vestigial and β-galactosidase regulated by escargot enhancer were found as well as in wild-type embryos. However, in escargot snail double mutant embryos, wing development proceeded until stage 13, but the marker expression was not maintained in later stages, and the invagination of the primordium was absent. From such analyses, it was concluded that Escargot and Snail expression in the wing disc are maintained by their auto- and crossactivation. Ubiquitous escargot or snail expression induced from the hsp70 promoter rescued the escargot snail double mutant phenotype with the effects confined to the prospective wing cells. Similar DNA binding specificities of Escargot and Snail suggest that they control the same set of genes required for wing development. We thus propose the following scenario for early wing disc development. Prospective wing cells respond to the induction by turning on escargot and snail transcription, and become competent for regulation by Escargot and Snail. Such cells initiate auto- and crossregulatory circuits of escargot and snail. The sustained Escargot and Snail expression then activates vestigial and other target genes that are essential for wing development. This maintains the commitment to the wing cell fate and induces wing-specific cell shape change.
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References
44
[1]
Alberga "The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers" Development (1991) 10.1242/dev.111.4.983
[2]
Ashburner "The genetics of a small chromosome region of Drosophila melanogaster containing the structural gene for alcohol dehydrogenase. IV: Scutoid, an antimorphic mutation" Genetics (1982) 10.1093/genetics/102.3.401
[3]
Bate "The embryonic origin of imaginal discs in Drosophila" Development (1991) 10.1242/dev.112.3.755
[4]
Bienz "Domain of Ultrabithorax expression in Drosophila visceral mesoderm from autoregulation and exclusion" Nature (1988) 10.1038/333576a0
[5]
Boulay "The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers" Nature (1987) 10.1038/330395a0
[6]
Carroll "Homeotic genes and the regulation and evolution of insect wing number" Nature (1995) 10.1038/375058a0
[7]
Cohen "Allocation of the thoracic imaginal primordia in the Drosophila embryo" Development (1993) 10.1242/dev.117.2.597
[8]
Cohen "Specification of limb development in the Drosophila embryo by the positional cues from segmentation genes" Nature (1990) 10.1038/343173a0
[9]
Cohen "Imaginal disc development" (1993)
[10]
Cohen "Proximal-distal pattern formation in Drosophila: graded requirement for Distal-less gene activity during limb development" Roux’s Arch. Dev. Biol (1989) 10.1007/bf02438941
[11]
DiNardo "Two-tiered regulation of spatially patterned engrailed gene expression during Drosophila embryogenesis" Nature (1988) 10.1038/332604a0
[12]
Ferguson "decapentaplegic acts as a morphogen to organize dorso-ventral pattern in the Drosophila" Cell (1992) 10.1016/0092-8674(92)90514-d
[13]
Frasch "Molecular analysis of even-skipped mutants in Drosophila development" Genes Dev (1988) 10.1101/gad.2.12b.1824
[14]
Fuse "Diploidy of Drosophila imaginal cells is maintained by a transcriptional repressor encoded by escargot" Genes Dev (1994) 10.1101/gad.8.19.2270
[15]
Grau "Mutations and chromosomal rearrangements affecting the expression of snail, a gene involved in embryonic patterning in Drosophila melanogaster" Genetics (1984) 10.1093/genetics/108.2.347
[16]
Gray "Short-range repression permits multiple enhancers to function autonomously within a complex promoter" Genes Dev (1994) 10.1101/gad.8.15.1829
[17]
Hartenstein "Studying Drosophila embryogenesis with P-lacZ enhancer trap lines" Roux’s Arch. Dev. Biol (1992) 10.1007/bf00188752
[18]
Hay "Expression of baculo virus P35 prevents cell death in Drosophila" Development (1994) 10.1242/dev.120.8.2121
[19]
Hayashi "A Cdc2 dependent checkpoint maintains diploidy in Drosophila" Development (1996) 10.1242/dev.122.4.1051
[20]
Hayashi "Control of imaginal cell development by the escargot gene of Drosophila" Development (1993) 10.1242/dev.118.1.105
[21]
Hiromi "Regulation and function of the Drosophila segmentation gene fushi tarazu" Cell (1987) 10.1016/0092-8674(87)90523-x
[22]
Ip "The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo" Genes Dev (1992) 10.1101/gad.6.9.1728
[23]
Jan "HLH proteins, fly neurogenesis, and vertabrate myogenesis" Cell (1993) 10.1016/0092-8674(93)90525-u
[24]
Kassis "Unusual properties of regulatory DNA from the Drosophila engrailed gene: three ‘pairing-sensitive’ sites within a 1. 6-kb region" Genetics (1994) 10.1093/genetics/136.3.1025
[25]
Lewis "A gene complex controlling segmentation in Drosophila" Nature (1978) 10.1038/276565a0
[26]
Lindsley (1992)
[27]
Mann "engrailed-mediated repression of Ultrabithorax is necessary for the parasegment 6 identity" Development (1994) 10.1242/dev.120.11.3205
[28]
Arias "Development and patterning of the larval epidermis of Drosophila" (1993)
[29]
Oda "Identification of a Drosophila homologue of α-catenin and its association with the armadillo protein" J. Cell Biol (1993) 10.1083/jcb.121.5.1133
[30]
Padget "A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family" Nature (1987) 10.1038/325081a0
[31]
Ray "The control of cell fate along the dorsal-ventral axis of the Drosophila embryo" Development (1991) 10.1242/dev.113.1.35
[32]
Rijsewijk "The Drosophila homologue of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless" Cell (1987) 10.1016/0092-8674(87)90038-9
[33]
Roark "scratch, a pan-neural gene encoding a zinc finger protein related to snail, promotes neuronal development" Genes Dev (1995) 10.1101/gad.9.19.2384
[34]
Rubin "Genetic transformation of Drosophila with transposable element vectors" Science (1982) 10.1126/science.6289436
[35]
Sauer "Concentration dependent transcriptional activation or repression by Krüuppel from a single binding site" Nature (1991) 10.1038/353563a0
[36]
Simcox "Establishment of imaginal discs and histoblast nests in Drosophila" Mech. Dev (1991) 10.1016/0925-4773(91)90087-m
[37]
Simcox "Imaginal discs can be recovered from cultured embryos mutant for the segment-polarity genes engrailed, naked and patched but not from wingless" Development (1989) 10.1242/dev.107.4.715
[38]
Simpson "Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos" Genetics (1983) 10.1093/genetics/105.3.615
[39]
Thummel "New CaSpeR P-element vectors" Drosophila Information Newsletter (1991)
[40]
Vachon "Homeotic genes in of the bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less" Cell (1992) 10.1016/0092-8674(92)90513-c
[41]
Whiteley "The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes" Mech. Dev (1992) 10.1016/0925-4773(92)90063-p
[42]
Williams "Control of Drosophila wing and haltere development by the nuclear vestigial gene product" Genes Dev (1991) 10.1101/gad.5.12b.2481
[43]
Younossi-Hartenstein "Embryonic origin of the imaginal discs of the head of Drosophila melanogaster" Roux’s Arch. Dev. Biol (1993) 10.1007/bf00539891
[44]
Zecca "Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing" Development (1995) 10.1242/dev.121.8.2265
Metrics
68
Citations
44
References
Details
- Published
- Apr 01, 1996
- Vol/Issue
- 122(4)
- Pages
- 1059-1067
- License
- View
Authors
Cite This Article
Naoyuki Fuse, Susumu Hirose, Shigeo Hayashi (1996). Determination of wing cell fate by the escargot and snail genes in Drosophila. Development, 122(4), 1059-1067. https://doi.org/10.1242/dev.122.4.1059
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