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Determination of Wing Cell Fate by the Escargot and Snail Genes in Drosophila

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Determination of Wing Cell Fate by the Escargot and Snail Genes in Drosophila Development 122, 1059-1067 (1996) 1059 Printed in Great Britain © The Company of Biologists Limited 1996 DEV5054 Determination of wing cell fate by the escargot and snail genes in Drosophila Naoyuki Fuse1,2,*, Susumu Hirose2 and Shigeo Hayashi1,4,† 1Genetic Stock Research Center, 2Department of Developmental Genetics, National Institute of Genetics, Mishima, Shizuoka-ken 411, Japan *Present address: Department of Molecular Biology and Genetics, Johns Hopkins University, School of Medicine, Baltimore, MD 21205, USA †Author for correspondence (e-mail: [email protected]) SUMMARY Insect appendages such as the wing and the leg are formed expression induced from the hsp70 promoter rescued the in response to inductive signals in the embryonic field. In escargot snail double mutant phenotype with the effects Drosophila, cells receiving such signals initiate developmen- confined to the prospective wing cells. Similar DNA binding tal programs which allow them to become imaginal discs. specificities of Escargot and Snail suggest that they control Subsequently, these discs autonomously organize patterns the same set of genes required for wing development. We specific for each appendage. We here report that two related thus propose the following scenario for early wing disc transcription factors, Escargot and Snail that are expressed development. Prospective wing cells respond to the in the embryonic wing disc, function as intrinsic determi- induction by turning on escargot and snail transcription, nants of the wing cell fate. In escargot or snail mutant and become competent for regulation by Escargot and embryos, wing-specific expression of Snail, Vestigial and β- Snail. Such cells initiate auto- and crossregulatory circuits galactosidase regulated by escargot enhancer were found as of escargot and snail. The sustained Escargot and Snail well as in wild-type embryos. However, in escargot snail expression then activates vestigial and other target genes double mutant embryos, wing development proceeded until that are essential for wing development. This maintains the stage 13, but the marker expression was not maintained in commitment to the wing cell fate and induces wing-specific later stages, and the invagination of the primordium was cell shape change. absent. From such analyses, it was concluded that Escargot and Snail expression in the wing disc are maintained by Key words: wing development, escargot, snail, cell fate their auto- and crossactivation. Ubiquitous escargot or snail maintenance, autoregulation, crossregulation, Drosophila INTRODUCTION signals that allocate the leg primordium within the ectodermal field established by the activities of segment polarity genes. In During development, groups of cells assume specific fates support of this idea, Simcox et al. (1989) used the embryo in according to positional information. Two mechanisms, vivo culture technique to show that wg is essential for the extrinsic induction and intrinsic determination, are required for formation of imaginal discs. Using a temperature sensitive wg these processes. Cells receiving inductive signals begin to allele, Cohen et al. (1993) demonstrated that the Dll expression express intrinsic determinants, acquire a specific cell fate, and in the leg primordium requires wg activity at about 5 hours of differentiate to form specific patterns autonomously. One development, roughly corresponding to the time when the rows example is imaginal discs of Drosophila (Cohen, 1993). In of wg and dpp expression overlap. dpp has been shown to exert embryos, each imaginal primordium is allocated to a specific a strong organizing activity in the establishment of the position in the ectoderm and invaginates to form a sac-like embryonic dorsoventral axis and in patterning imaginal discs imaginal disc. Subsequently, each performs a series of (Ferguson and Anderson, 1992; Zecca et al., 1995), but its role autonomous events to organize adult external structures. in imaginal disc induction needs to be further studied. The disc The first sign of imaginal disc induction is the expression of development continues after the overlap between Dll the homeobox gene Distal-less (Dll) in the prospective leg expression and the intersection of the wg and dpp rows are lost imaginal disc (Cohen, 1990). In stage 11 embryos, the leg (Cohen et al., 1993), suggesting that the induced cells must primordia, visualized by the Dll RNA expression, appears in activate an intrinsic determinant to irreversibly commit them clusters of cells that overlap the intersection between the to imaginal cell fate. Ventral leg and dorsal wing primordia dorsoventral row of cells expressing the segment polarity gene appear to originate from a common imaginal primordium. The wingless (wg) and the anterior-posterior row of decapenta- cell lineage tracing study has shown that in stage 12, the wing plegic- (dpp) expressing cells (Cohen et al., 1993). Since Wg disc cells expressing vestigial (vg) segregate and move dorsally and Dpp are secreted signaling molecules (Padget et al., 1987; away from Dll-expressing cells (Cohen et al., 1993). Rijsewijk et al., 1987), they were proposed to be the inductive Although the intersection between wg- and dpp-expressing 1060 N. Fuse, S. Hirose and S. Hayashi rows exist in all the trunk segments, wings and legs form only studied the function of two closely linked genes, escargot in the thorax. This was shown to be due to the negative regula- (snail) and snail (sna). esg and sna encode transcriptional reg- tion by homeotic genes. In the abdomen, genes in the bithorax ulators with similar C2H2 type zinc finger domains (76% amino complex repress leg and wing formation (Bate and Martinez acid identity; Boulay et al., 1987; Whiteley et al., 1992). esg Arias, 1991; Simcox et al., 1991; Vachon et al., 1992; Carroll et is expressed in most imaginal primordia found in the embryo al., 1995) and in the first thoracic segment, wing formation was repressed by the Sex comb reduced gene in the Antennapedia complex (Carroll et al., 1995). In embryos mutant for Antenna- pedia, which is responsible for the identity of parasegment 4 and 5, formation of the leg and wing primordium was detectable (Mann, 1994; Carroll et al., 1995), suggesting that these appendages are formed as a default in the ‘ground state’ of segmental identity (Lewis, 1978). We must therefore seek a putative intrinsic determinant of imaginal disc formation outside the homeotic gene complex. The nuclear proteins, Dll and Vg are the earliest known markers for the leg and wing imaginal discs, and are required for pattern formation along the PD axis in the adult (Cohen and Jürgens, 1989; Cohen, 1990; Williams et al., 1991). However, their involvement in imaginal disc formation is not clear since imaginal discs are formed in the absence of Dll or vg (Williams et al., 1991; Cohen et al., 1993). To identify an intrinsic determinant of the imaginal disc, we Fig. 2. Esg and Sna are expressed in the wing primordium. Wild type embryos double-stained with anti-Esg (green) and anti-Sna (red) antibodies. All embryos are oriented as dorsal up and anterior to the left. (A) In a stage 5 embryo, Sna is expressed in the ventral region, the Fig. 1. Esg and Sna have similar DNA binding specificities. prospective mesoderm. Esg is expressed in the dorsal region. There is (A,B) DNA binding specificities of Esg (A) and Sna (B). no overlap, demonstrating the specificity of each antibody. (B) In a Recombinant GST-Esg and GST-Sna fusion proteins bind to 32P- stage 13 embryo, Esg and Sna begin to be expressed in wing (w) and labeled DNA containing the E2 box. Addition of unlabeled DNA haltere (h) primordia which appear yellow (arrowheads). (C) In a stage containing wild-type (closed circle) or mutant E2 box sequences 15 embryo, wing (w), haltere (h) and genital (g) discs are stained (others) competed with this binding. Amounts of probe DNA bound yellow, indicating colocalization of Esg and Sna proteins. to the proteins expressed as percentages relative to the control (D) Enlarged view of a wing and a haltere disc which expressed both without specific competitor (Y-axis) were plotted against the ratio of Esg and Sna. An anterior spiracle (a) expressed only Esg. (E) Ventral competitor to probe (X-axis). The competition profiles of Esg (A) part of the same embryo as shown in D. From left to right, a pair of the and Sna (B) are very similar. (C) Oligonucleotide sequences used as first thoracic leg disc and a second and a third leg disc (slightly out of competitors. Central parts of the 24 mer double strand focus) are seen. The majority of leg disc cells express only Esg. A oligonucleotides are shown. Sequences corresponding to the Esg small subset of leg disc cells expressing both Esg and Sna are binding consensus (Fuse et al., 1994) are underlined. indicated by arrowheads. Bar, 125 µm for A-C and 45 µm for D and E. Overlapping activity of zinc finger proteins 1061 Fig. 3. esg and sna are required for Sna expression in the wing disc. All embryos were stained with anti-Sna antibody. (A) Stage 15 control embryo (sna1/CyO). (B) esgG66B embryo. Wing (arrowhead, w), haltere (h) and genital (g) discs express Sna as in the control (A). (C) Ventral view of a sna1 embryo. sna1 mutation causes the malformation of the whole body, but the wing, haltere and genital discs express the truncated Sna protein. (D) Ventral view of an esgG66B sna1 embryo. Sna expression in the wing, haltere and genital discs is abolished. (E) Ventral view of a heat treated esgG66B sna1 HSesg embryo. Sna expression is restored in the wing and haltere discs (arrowhead). (F,G) High magnification views of the wing disc in stage 15-16 embryos. (F) Control embryo (esgG66B sna1/CyO). Sna-expressing cells invaginate to form a sac-like wing disc. (G) An example of heat shock treated esgG66B sna1 HSesg embryo. Such embryos showed a wide range of wing disc phenotype from no invagination at all to nearly complete invagination shown here.
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