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First published online August 4, 2003
doi: 10.1242/10.1242/dev.00643

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The Pax-homeobox gene eyegone is involved in the subdivision of the thorax of Drosophila

Centro de Biología Molecular CSIC-UAM, Universidad Autónoma de Madrid, 28049 Madrid, Spain

View larger version (7K): [in a new window]   Fig. 1. Molecular map of the eyg/toe genomic region. The three transcription units located in the region (eyg, toe and CG3212) are shown as boxes, and their transcriptional orientation is indicated by arrows. The location of the EM461Gal4 insert with respect to the genes is also indicated. As shown, neither the eygSA1 nor the eygSA2 deletions eliminate toe, which is located 30 kb downstream from eyg.

View larger version (112K): [in a new window]   Fig. 3. Phenotype of eyg mutants. (A) Adult thorax of an eygSA2/Df(3L) iro fly. The scutellum (sc) is present, as well as some of the lateral macrochaetes, but most or all the eyg domain is missing. Note the very low number of microchaetes, which compose most of the eyg domain (compare with Fig. 1A,B). (B,C) Anti-Eyg antibody of the thoracic region of a wild-type disc (B) and a eygSA2/eyg20MD1-mutant disc (C). Low levels of anti-Eyg staining can still be observed in the mutant disc, suggesting that the antibody also recognises the Toe protein. (D) eyg expression at late embryogenesis of a wild-type embryo, as revealed by in situ hybridisation with a specific eyg probe. (E) In situ hybridisation using a specific toe probe reveals a similar expression pattern. (F) In eygSA2-mutant embryos there is no detectable eyg transcription. (G) In eygSA2-mutant embryos toe transcription appears normal. (H,I) Adult thorax of a fly of genotype eygGal4-gv5/Df(3L)iro (H), showing a phenotype very similar to that of the fly in A. The high levels of toe activity in eygGal4-gv5/Df(3L)iro > UAS-toe flies (I) give rise to a partial rescue of the mutant phenotype. Note the appearance of dorsocentral bristles and of numerous microchaetes.

View larger version (78K): [in a new window]   Fig. 2. Expression domain of eyg in the adult mesothorax and the wing imaginal disc. (A) Adult mesothorax of a fly of genotype eyg-Gal4 > UAS-lacZ stained with X-Gal (blue). The eyg domain occupies most of the notum, except the scutellum (sc) and the lateral region, which includes some macrochaetes. The dorsocentral bristles are marked with arrows and the scutellar bristles with arrowheads. (B) Early (left) and mature (right) wild-type third instar wing discs stained for en (green) and eyg (red). The eyg expression domain occupies the greater part of the anterior compartment, but does not extend to the posterior compartment. Note the dot of expression in the wing hinge. (C) The thoracic region of a wild-type disc stained for neuralizer (neu; green), which marks the precursors of the macrochaetes, and eyg (red). The precursors of two dorsocentral bristles (arrows), as well as some of the pre-sutural ones, are inside the eyg domain. The scutellar bristles (arrowheads) and the more lateral ones are outside the eyg domain. (D) Double staining for pnr (blue) and eyg (red), showing the overlap of their expression domains. (E) Thoracic region of a wild-type wing disc doubly stained for Iro genes (green) and eyg, showing that the expression domains of the genes overlap in part.

View larger version (111K): [in a new window]   Fig. 4. Phenotypic consequences of ectopic eyg and toe expression. The expression of the different Gal4 lines driving UAS-LacZ or UAS-GFP is shown in the insets. (A) Notum of a fly of genotype 248-Gal4 > UAS-eyg. The scutellum is transformed toward scutum as indicated by the change of morphology and the presence of microchaetes in the posterior notum. Note the opposite polarity of the bristles in the transformed and untransformed territories. (B) Transformation observed in the notum of 248-Gal4 > UAS-toe flies, resembling that portrayed in A. (C) Notum of a 638-Gal4 > UAS-toe fly. The ectopic expression of toe is limited to the scutellum region (arrow in inset), which differentiates microchaetes (arrow). (D) Similar transformation found in 455-Gal4 > UAS-eyg. The driver directs expression to the scutellum region (inset). (E) The broader expression (inset) of eyg in the posterior notum region produces more extensive transformation. (F) In ap-Gal4 > UAS-eyg flies the Eyg product is uniformly expressed in all the notum cells. It results in an expansion of the normal anterior-central region of the notum, and the disappearance of the scutellum and the lateral region.

View larger version (44K): [in a new window]   Fig. 5. Ectopic eyg expression. (A) The 638-Gal4 line drives expression in the posterior thorax and the wing pouch (arrows). (B) In 638-Gal4 > UAS-eyg there is a clear transformation of the scutellum towards scutum (thick arrow), but there is little transformation in the wing, except in the centre (thin arrow), where there is some transformation towards notum. (C) Thorax of a fly of genotype 638-Gal4 > UAS-ara. The wing is replaced by a duplication of the notum (DN). (D) Thorax of a fly of genotype 638-Gal4 > UAS-eyg UAS-ara. The wing is replaced by a notum duplication (DN), but the scutellar regions of the normal and the duplicated notum are transformed towards scutum (thick arrow). Note the presence of microchaetes, which are indicative of the transformation.

View larger version (131K): [in a new window]   Fig. 6. Regulation of eyg by the Iro and pnr genes. (AC) Large Iro gene-mutant clone (black; arrows) induced at first instar. The cells of the clone show no eyg expression, and the effect extends to wild-type cells close to the clone. (D-F) Thoracic region of a wing disc containing clones deficient for Iro gene activity (black). The medial region is to the left and the lateral is to the right. The clones located towards the lateral region (arrows) lose eyg expression (blue), whereas those located more medially (arrowheads) do not. (G) Wing disc of 638-Gal4 > UAS-ara showing that the ectopic ara expression induces eyg activity (red). (H) 638-Gal4 > UAS-pnr wing disc also showing activation of eyg by pnr.

View larger version (68K): [in a new window]   Fig. 7. Negative regulation of eyg by Hh signalling. (A-C) Clone of cells mutant for smo (arrow; marked black in B) showing gain of eyg activity (red). (D) A smo clone marked with yellow (arrow) in the adult cuticle. An amplification is shown in the lower panel. The clone differentiates notum structures resembling the scutum, as indicated by the microchaetes. (E-G) Clones mutant for ptc (arrows) exhibit loss of eyg expression.

View larger version (139K): [in a new window]   Fig. 8. Negative regulation of eyg by Dpp signalling. (A-C) Derepression of eyg in Mad-mutant clones (black). Note that in the larger clone (arrow), eyg (red) is activated only in the cells closer to the eyg domain. (D-F) Two Mad clones (arrows), a small one close to the eyg domain, showing ectopic eyg activation, and a larger one in the posterior compartment, in which eyg is not activated. Note the increase of eyg expression in the mad clone close to the border (arrowhead). (G-I) Several clones mutant for a constitutive form of the Tkv receptor, showing repression of eyg.