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Dpp and Hh signaling in the Drosophila embryonic eye field

Department of Molecular Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA 90095, USA

View larger version (28K): [in a new window]   Fig. 1. Topology of the anterior brain/eye anlage (green) and eye field (magenta) in vertebrates (A) and Drosophila (B,C). (A,B) The fate map of the head structures before neurulation (dorsal view). Map positions of main neural structures of the head are indicated. (C) The progenitors of the Drosophila brain and visual system at a later stage when the visual primordium has split into larval and adult eye, and inner/outer optic lobe.

View larger version (83K): [in a new window]   Fig. 2. The Drosophila anterior brain/eye anlage and its derivatives. (A) Map of the anterior brain/eye anlage around gastrulation (lateral view, anterior towards the left, dorsal upwards). Positions of various head derivatives and landmark structures are indicated (bo, larval eye (Bolwig’s organ); cc, corpora cardiaca; cf, cephalic furrow; eye, adult eye; fg, foregut; he, dorsal head epidermis; oli, inner optic lobe (lobula complex); olo, outer optic lobe (medulla and lamina); pr, protocerebral neurectoderm). (B,C) Expression of orthodenticle (otd) at the onset of gastrulation (stage 6, B) and at the extended germband stage (stage 11, C; both panels show whole-mount in situ hybridization using an otd cDNA probe). Note widespread early expression of otd in the entire anterior brain/eye anlage. Later expression becomes restricted to the protocerebrum. (D,E) Lateral view (D) and dorsal view (E) of stage 15 embryo labeled with anti-FasII, which visualizes founder tracts of the brain (br) and ventral nerve cord (vc), as well as the corpora cardiaca (cc) and thin nerves (arrow in E) connecting the corpora cardiaca with the pars intercerebralis (pi) of the brain. Dorsal head epidermis (he) is in the process of involuting to form the dorsal pouch (dp). (F) Stage 12 embryo, lateral view, expressing lacZ under the control of the glass promoter in the precursors of the corpora cardiaca (cc). These cells have just separated from the dorsal aspect of the foregut primordium (fg). (G) Lateral view of stage 15 embryo labeled with anti-FasII. In this more lateral plane of focus, the larval eye (bo) and outer optic lobe (olo) are visible. Small placode dorsal of the larval eye represents the primordium of the adult eye (eye).

View larger version (107K): [in a new window]   Fig. 3. Expression of dpp and its antagonists, sog and brk, in the head region of the early embryo. All panels show lateral view of embryo whole-mounts labeled by antibody or in situ hybridization with the probes of the corresponding genes (indicated in at bottom right). Stages are indicated at the right. (A) Blastoderm stage. dpp expression in dorsal region of trunk and head. (B,C) Gastrulation. Antibody against pMAD shows activation of Dpp pathway in the visual primordium (vp). B, dorsal view; C, lateral view. (D) Late gastrulation and early extended germ band. dpp expression has ceased in most of the head, except posterior rim of visual primordium (arrow). (E) Late extended germband. Dpp is expressed in small discrete spots in the dorsal midline and anterior to the larval eye (arrow). (F) Expression of sog in the ventral blastoderm of the trunk and head region. (G) Around gastrulation, sog expression expands from the ventral ectoderm (ve) into the domain of the protocerebrum (pr). (H,I) Low level expression of sog and brk in the stage 10 protocerebral neurectoderm. (J) In a sog; brk double mutant, expression of dpp is expanded into the entire ventral neurectoderm (ve; compare this image with G), but not the protocerebral neurectoderm (pr). cf, cephalic furrow; de, dorsal trunk ectoderm.

View larger version (90K): [in a new window]   Fig. 4. Phenotypic effects of reduction in Dpp function. (A,B) Dorsal view of stage 11 wild-type (A) and dpp hypomorph, dppE87 (B), embryo labeled with a cDNA probe for the race gene, a downstream target of Dpp expressed in the amnioserosa (as) and dorsal head epidermis (he). Note absence of race (arrows) in the dpp hypomorph (B). (C,D) Dorsal view of stage 13 embryo (C, wild type; D, dppE87) in which outer optic lobe (ol) and larval eye (bo) are labeled by anti-Fas II (violet) and mAb22C10 (brown), respectively. In the dpp hypomorph, the dorsal midline has been transformed into visual primordium, resulting in an unpaired median larval eye and optic lobe (cyclops). (E,F) Dorsal view of stage 10 wild-type (E) and dppE87 (F) labeled with probe for the eya gene. eya is expressed in a complex pattern in the anterior protocerebrum, visual primordium (vp) and, at lower level, dorsal head epidermis (he; outlined by arrows and a broken line). The head epidermis is missing in dppE87 (arrows)

View larger version (65K): [in a new window]   Fig. 5. Phenotypic effects of loss of Dpp function and da-Gal4-directed overexpression of dpp. (A,B) Lateral view of stage 13 wild-type (A) and dpp-null (B) embryos labeled with anti-FasII. Note absence of optic lobe and larval eye (ol/bo in A) in the mutant (arrow in B). (C,D) Dorsal view of stage 9 wild-type (C) and dpp-null (D) embryos labeled with anti-Snail, which recognizes protocerebral neuroblasts (pn). In the mutant, dorsal head ectoderm is ‘invaded’ by protocerebral neuroblasts. (E,F) Dorsal view of stage 11 wild-type (E) and dpp-null (F) embryos labeled with a probe for the ind gene that is expressed in the anterior lip of the optic lobe and a group of neuroblasts delaminating from this domain (oln). In the wild type, the oln neuroblasts occupy a lateral position; in the mutant, they appear dorsomedially. (G,H) Dorsal view of stage 15 wild-type (G) and da-Gal4; UAS-dpp embryos (H) labeled with probe for race. Note widening of dorsomedial strip of race-positive head epidermis (he). (I) Lateral view of stage 10 da-Gal4; UAS-dpp embryo, showing expansion of amnioserosa (as). (J) Lateral view of stage 14 da-Gal4; UAS-dpp embryo labeled with anti-FasII (brown) and mAb22C10 (purple) to visualize larval eye (bo) and optic lobe (ol). Both structures are of normal size but displaced ventrally. Epidermis of clypeolabrum (cl) and dorsomedial head (he) has expanded. ao, antennal organ; gn/ae, gnathal segments and anterior endoderm.

View larger version (82K): [in a new window]   Fig. 6. Dpp controls the expression of the head gap genes otd (A,B) and tll (C,D), as well as the early eye genes so (E,F) and eya (G,H). All panels show dorsal view of stage 10 embryos labeled with cDNA probes for the corresponding genes. (A,C,E,G) Wild-type controls; (B,D,F,H) dpp-null embryos. Both otd and tll, normally excluded from the dorsal midline (A,C), are expressed in the dorsal midline in dpp mutants (B,D). Expression of both so and eya in the visual primordium (vp) is abolished in dpp mutants (arrows in F,H), although anterior head expression is preserved.

View larger version (111K): [in a new window]   Fig. 7. Requirement of zerknuellt (zen) during head patterning. (A) Dorsal view of stage 6/7 embryo labeled by in situ hybridization, showing expression of zen in primordium of dorsal head epidermis (he). (B) Dorsal view of stage 15 zen mutant embryo labeled with anti-FasII, showing cyclopic optic lobe (ol). (C,D) Expression of so in the dorsal head of a stage 11 wild-type (C) and zen mutant (D) embryo. Note high level of so in dorsal midline (arrow) in the mutant, compared with wild type where so labels the laterally migrated visual primordia (vp). (E) Dorsal view of stage 10 zen mutant embryo labeled with in situ probe against tll, showing persistence of tll in dorsal midline (compare with Fig. 6, showing wild-type expression of tll). (F) Model illustrating the role of Zen as repressor of early regulatory genes (exemplified by so) in the dorsal midline.

View larger version (117K): [in a new window]   Fig. 8 Expression of hh and ptc in the embryonic head. All panels show lateral views of embryos labeled with a cDNA probe for hh (left column; A-C) and ptc (right column; D-F). Embryo in B also expressed a so-lacZ construct in the visual primordium (brown, vp). (A,D) Stage 7; (B,E) stage 9; (C,F) stage 11. an, antennal stripe; bo, larval eye; cf, cephalic furrow; md, mandibular stripe; mx, maxillary stripe; ola, anterior lip of optic lobe invagination; olp, posterior lip of optic lobe invagination; pra, pre-antennal stripe; vp, visual primordium.

View larger version (89K): [in a new window]   Fig. 9. Phenotypic effects of loss and overactivity of Hh signaling in the embryonic head. (A) Dorsal view of stage 15 wild-type embryo labeled with mAb 22C10 to visualize larval eye (bo). (B) ptc-null embryo at same stage and orientation as A. Note cyclopic pattern and increased size of larval eye (bo). (C) Lateral view of stage 15 hh mutant embryo labeled with mAb22C10. The larval eye, normally dorso-posterior of the antennal organ (ao) is absent (arrow). (D) Dorsal view of stage 16 embryo in which a hs-hh construct was activated during 3-5 hours of development. Larval eye and optic lobe are labeled with anti-FasII. Early overexpression of hh results in cyclopic optic lobe.(E, F) Dorsal view of stage 12 wild-type (E) and hh-null (F) embryos labeled with an eyeless probe. In wild type, ey expression begins at this stage in the primordium of the adult eye (eye) which is right in front of the optic placode (op). Note absence of ey expression in the mutant (arrow in F). (G,H) Dorsal view of stage 16 wild-type (G) and hh-null (H) embryos. Beside mushroom body (mb) and other neural foci, ey is expressed in the lateral rim of the dorsal pouch which represents the eye primordium (eye). This expression domain is absent in the mutant (arrow in H). br, brain.

View larger version (95K): [in a new window]   Fig. 10. (A,B) Expression of pMAD (purple) in visual primordium (arrows) of stage 7 wild-type (A; note brown Ftz stripes caused by the presence of ftz-lacZ on balancer chromosome) and hh-null (B) embryos. (C,D) Whole-mount in situ hybridization of stage 7 embryos, showing expression of hh (C) and ptc (D) in visual primordium (arrows) of dpp-null mutant. (E,F) Expression of Ci in eye primordium (arrows) of stage 7 wild-type (E) and dpp-null (F) embryos.

View larger version (51K): [in a new window]   Fig. 11. Model of the function of Dpp and Hh signaling in the Drosophila embryonic head, explaining the mechanism that results in the development of a cyclops phenotype in different genetic backgrounds. Each row (A-C) shows dorsal view of head at blastoderm stage (left panel) and after gastrulation (right panel). (A) Wild type; (B) loss of Ptc or overexpression of Hh; and (C) reduction of Dpp. For details, see Discussion.

View larger version (35K): [in a new window]   Fig. 12. (A) Comparison of eye morphogenesis in a vertebrate (left column) and insect (right column). All panels represent schematic cross-sections of the head region of the embryo. First row shows anterior brain/eye anlage before neurulation. The second and third row depict the derivatives of this anlage after neurulation and in the mature organism, respectively. For details, see Discussion. (B) Evolution of chordate body plan by dorsoventral axis reversal. According to this hypothesis, bilaterian ancestor had a ventral nervous system. (C) Evolution without axis reversal. This alternative hypothesis suggests that ancestor had only anterior brain. Separate lines of evolution added a trunk nervous system dorsally (chordates) or ventrally (arthropods).