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The Sox-domain containing gene Dichaete/fish-hook acts in concert with vnd and ind to regulate cell fate in the Drosophila neuroectoderm

¹ Program in Molecular Cell Biology, Washington University School of Medicine, 4566 Scott Avenue, St Louis, MO 63110, USA
² Department of Genetics, Washington University School of Medicine, 4566 Scott Avenue, St Louis, MO 63110, USA

View larger version (131K): [in a new window]   Fig. 1. Egfr maintains vnd expression in the medial column. High magnification ventrolateral and ventral views of wild-type (A,C,E) and Egfr (DER; B,D,F) embryos labeled for vnd expression. Insets in E,F show high-magnification lateral views of vnd expression in stage 10 wild-type and Egfr embryos. (A,B) During stage 6, vnd expression becomes detectable in an approx. six-cell-wide column on either side of the ventral midline in wild-type and Egfr embryos. (C) By late stage 8 in wild-type embryos, vnd expression narrows to a three-cell-wide column on either side of the ventral midline. These cells identify the medial column and stage 10 embryos (E) maintain this pattern of vnd expression. Inset in E shows that neuroectodermal cells (arrow) and NBs (arrowhead) express vnd. (D) In Egfr mutant embryos, vnd expression begins to dissipate in the ventral neuroectoderm by stage 8 (arrows) and by stage 10 (F) vnd expression is completely absent from the neuroectoderm. Inset in F shows that NBs (arrowhead) but not neuroectodermal cells (arrow) express vnd in Egfr mutant embryos. Anterior is towards the left and the line indicates the ventral midline.

View larger version (163K): [in a new window]   Fig. 2. Egfr regulates DV pattern in the neuroectoderm through genes other than vnd and ind. High-magnification ventral views of the neuroectoderm of stage 9 (A-C) and late stage 8 (D-I) wild-type (A,D), ind (B,E), Egfr (DER; C,F), vnd; ind (G), vnd; Egfr (vnd;DER; H) and vnd; Dichaete ind (I) mutant embryos labeled for NBs (A-C) or msh expression (D-I). (A) In wild-type embryos, NBs occupy three columns: medial (m), intermediate (i) and lateral (l). (B) In ind embryos, intermediate NBs do not form and medial and lateral NBs are separated by a gap (bracket and arrows). (C) In Egfr embryos, intermediate NBs do not form and medial and lateral NBs reside adjacent to each other (arrows). (D) In wild-type embryos, msh expression is restricted to the lateral column. (E) In ind embryos msh expression expands into the intermediate column. (F) In Egfr embryos, msh expression expands into the intermediate column and partially into the medial column. (G) In vnd; ind embryos, msh is expressed throughout the neuroectoderm with higher expression laterally (arrowheads) than ventrally (arrows). (H) In vnd; Egfr embryos and in (I) vnd; Dichaete ind embryos, msh is expressed uniformly throughout the neuroectoderm. Anterior is towards the left and the line indicates the ventral midline.

View larger version (103K): [in a new window]   Fig. 3. Dichaete is expressed in the medial and intermediate neuroectodermal columns and in lateral NBs. Low- (A) and high- (B-D) magnification ventral views of wild-type stage 8 (A,B) or stage 11 (C,D) embryos labeled for Dichaete (A), Dichaete (green) and msh (red) (B), or Dichaete (brown) and engrailed (blue) (C,D). (A) In wild-type embryos, Dichaete is expressed in the ventral region of the neuroectoderm. (B) The lateral limit of Dichaete expression abuts precisely the medial limit of msh expression in the lateral column (arrows). (C) In early stage 11 embryos, Dichaete expression persists in the medial and intermediate columns; however, lateral column NB 7-4 now expresses Dichaete (arrowhead). (D) In late stage 11 embryos two additional lateral column NBs (NB 2-5 and NB5-6) express Dichaete (arrows). Anterior is towards the left and the line indicates the ventral midline.

View larger version (135K): [in a new window]   Fig. 4. Dichaete regulates cell fate in the intermediate column. High-magnification ventral views of stage 9 wild-type (A-C), Dichaete (D-F) and Dichaete ind/ Dichaete + (G,H) mutant embryos labeled for ac (A,D,G) or ac (red) and ind (green; B,C,E,F,H). (A) In wild-type embryos ac is expressed in proneural cell clusters in the medial and lateral but not intermediate (arrows) columns of rows 3 and 7. (B,C) Normally, the expression of ind and ac is mutually exclusive in the neuroectoderm (arrows, B) and NBs (arrows, C). (D-F) In Dichaete embryos, ac expression is partially derepressed in the intermediate column (arrows, D) and intermediate column neuroectodermal cells (arrows, E) and NBs (arrows, F) inappropriately co-express ac and ind. (G,H) In Dichaete embryos heterozygous for ind, ac expression is strongly derepressed in the intermediate column (arrows, G) and ac and ind expression again colocalize in intermediate column neuroectodermal cells (arrows, H). Anterior is towards the left and the line indicates the ventral midline.

View larger version (149K): [in a new window]   Fig. 5. Dichaete regulates NB formation. High-magnification ventral views of stage 11 wild-type (A), Dichaete (B), vnd (C) and vnd; Dichaete (D) embryos labeled for Castor protein. (A) At stage 11 in wild-type embryos, a Castor-positive NB 6-1 forms in every hemisegment (arrows). (B) In Dichaete mutant embryos NB 6-1 forms in most hemisegments (arrows indicate Castor-positive NB6-1; arrowheads indicate the absence of NB6-1). (C) In vnd mutant embryos NB 6-1 forms in roughly one-third of all hemisegments (arrows); arrowhead indicates the absence of NB6-1. (D) In vnd; Dichaete double mutant embryos, NB 6-1 rarely forms (arrow); arrowheads indicate the absence of NB 6-1. Anterior is towards the left and the line indicates the ventral midline.

View larger version (117K): [in a new window]   Fig. 6. Egfr regulates Dichaete expression in the neuroectoderm. (A-D) Ventrolateral views of whole-mount stage 8 (A-D) and high-magnification ventral views of stage 11 (E-H) wild-type (A,E), vnd (B,F), Egfr (DER; C,G) and vnd; Egfr (vnd; DER; D,H) mutant embryos labeled for Dichaete. (A) In stage 8 wild-type embryos Dichaete is expressed in the medial and intermediate columns. (B) In vnd embryos, Dichaete expression is normal during stage 8. (C,D) In stage 8 in Egfr (C) or vnd; Egfr (D) embryos, Dichaete expression is strongly reduced in the intermediate column and moderately reduced in the medial column. (E) In stage 11 wild-type embryos, Dichaete is expressed in the medial and intermediate columns, and in one or more lateral column NBs. (F) In stage 11 vnd embryos, Dichaete is expressed in an irregular stripe two-to-four cells wide immediately adjacent to and on either side of the ventral midline (arrows). (G) In stage 11 Egfr embryos, Dichaete is expressed in an irregular stripe of cells zero to three cells wide immediately adjacent to and on either side of the midline (arrows). (H) In stage 11 vnd; Egfr embryos, Dichaete is not expressed in the neuroectoderm but is expressed in the ventral midline (arrowhead) and lateral NBs. Anterior is towards the left; white arrowheads (A-D) and lines (E-H) indicate ventral midline.

View larger version (16K): [in a new window]   Fig. 7. The genetic regulatory hierarchy that regulates DV pattern in the neuroectoderm (left) and the molecular pathway through which Dichaete, vnd and ind might regulate target gene expression (right). Left: Egfr stands atop the genetic pathway that regulates DV pattern in the neuroectoderm. Egfr activates ind in the intermediate column and Dichaete in the medial and intermediate columns, while maintaining vnd expression in the medial column. vnd is activated independently of Egfr and plays a supporting role in regulating Dichaete expression. Dichaete activity appears to converge with that of vnd in the medial column and that of ind in the intermediate column to regulate DV pattern and cell fate. Right: a model that proposes that physical interactions between Dichaete and Vnd, as well as Dichaete and Ind, mediate the ability of Dichaete to carry out distinct function in different columns. Other proteins (X/Y) are likely required in these processes.