spacer gif spacer gif spacer gif spacer gif spacer gif
 QUICK SEARCH:   [advanced]


spacer gif
     Home     Help     Feedback     Subscriptions     Archive     Search     Table of Contents    

First published online February 9, 2006
doi: 10.1242/10.1242/dev.02260


Development 133, 785-790 (2006)
Published by The Company of Biologists 2006


This Article
Right arrow Summary Freely available
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Related articles in Development
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Franch-Marro, X.
Right arrow Articles by Casanova, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Franch-Marro, X.
Right arrow Articles by Casanova, J.

Association of tracheal placodes with leg primordia in Drosophila and implications for the origin of insect tracheal systems

Xavier Franch-Marro1,*, Nicolás Martín1, Michalis Averof2,{dagger} and Jordi Casanova1,{dagger}

1 Institut de Biologia Molecular de Barcelona (CSIC), Parc Científic de Barcelona, C/Josep Samitier 1-5, 08028 Barcelona, Spain.
2 Institute of Molecular Biology and Biotechnology (IMBB), 71110 Iraklio Crete, Greece.


Figure 1
View larger version (116K):

[in a new window]
 
Fig. 1. Drosophila tracheal and leg primordia derive from closely associated populations of cells. (A) The Drosophila tracheal system visualized by the 2A12 antibody. (B) The tracheal system arises from 10 tracheal placodes (arrowheads on first and last placode) that express the trh gene; trh is also expressed in the salivary glands (sg). (C) Staining for trh in the tracheal placodes, and Dll in cephalic structures and leg primordia (arrows) in a stage 11 embryo. (D) Higher magnification view, showing the proximity of thoracic tracheal placodes and leg primordia. (E) Staining for trh expression (by means of an enhancer trap insertion in the gene) and btd expression in a stage 9/10 embryo. (F) Higher magnification view, showing the close apposition of trh- and btd-expressing cells.

 

Figure 2
View larger version (98K):

[in a new window]
 
Fig. 2. Induction of leg structures in the Drosophila larval abdomen. (A) Lateral view of a wild-type first instar larval cuticle. Arrows point to Keilin's Organs (KOs), the rudimentary larval legs that appear in the thoracic segments. (B) Ventral view of a cuticle upon ectopic expression in the abdomen of Dll and btd. Arrows point to KOs that develop in otherwise normal abdominal segments. (C) Detail of A showing a wild-type thoracic KO (arrows). (D) Detail of B, showing the KO developing in abdominal segments (arrows; abdominal segments 4 and 5; more than 85% of the scored abdominal hemisegments show these KOs; n=20 embryos). (E) High magnification of a wild-type KO. (F) High magnification of a thoracic KO upon btd overexpression. (G) High magnification of an abdominal KO upon btd and Dll overexpression. KOs upon btd overexpression have more than the three hairs seen in the wild type. (H) Scheme of the proposed interactions giving rise to appendage primordia.

 

Figure 3
View larger version (56K):

[in a new window]
 
Fig. 3. wg signalling provides a genetic switch for the specification of leg versus tracheal primordia. (A,B) Wild-type expression pattern of trh in the salivary glands and tracheal placodes, and of btd in cephalic segments and cell clusters in thoracic and abdominal segments. (C,D) In a wg mutant, trh expression is expanded along the anteroposterior axis, whereas btd expression is abolished in the thoracic and abdominal segments. (E,F) Conversely, upon ectopic expression of wg, trh expression in the tracheal placodes is suppressed and btd expression is expanded. (G,H) Restricted ectopic activation of the wg pathway reduces the domains of trh expression and expands those of btd expression. (I,J) Restricted inactivation of the wg pathway expands trh expression and reduces btd expression. All embryos are at stage 11. (K) Detail of wg mutant at a somewhat later stage, showing that the ectopic trh-expressing cells begin to invaginate. (L) Detail of an embryo at germ band extension upon ectopic expression of wg at germ band retraction, indicating that expansion of btd occurs only in part of the embryonic ectoderm, while the segmental pattern persists in the central nervous system. (M) Schematic representation of the role of wg (transcribed in the yellow domain) in promoting appendage and repressing tracheal fates.

 

Figure 4
View larger version (69K):

[in a new window]
 
Fig. 4. Similarities and hypothetical relationships between surfaces in crustaceans and insects. (A) Expression of Vvl in thoracic appendages of Artemia franciscana. Four appendages of increasing maturity are shown, immunochemically stained with an anti-Vvl antibody: (a) onset of Vvl expression; (b) early uniform Vvl expression; (c) the beginning of Vvl upregulation in the distal epipod/gill; and (d) higher levels of Vvl in the distal epipod of near-mature appendages. (B) Higher magnification of mature epipod, showing high levels and nuclear localization of Vvl. (C-E) Expression of trh and vvl in thoracic appendages of Parhyale hawaiensis, visualized by in situ hybridization. (C) Expression of Parhyale trh in thoracic appendages, showing strong staining in epipods but no staining in the endopods/legs. (D) Expression of Parhyale vvl at an early stage of appendage development, showing specific expression in the primordia of epipods. Cells are visualized by nuclear staining with DAPI. (E) Expression of Parhyale vvl at a late stage of appendage development. (F) Engrailed staining in the distal epipods/gills of the crayfish Pacifastacus leniusculus. The anterior gill comprises exclusively non-en-expressing cells (labelled A), whereas the posterior gill comprises both non-en- and en-expressing cells (labelled AP). (G) Nubbin/Pdm staining in the same epipods/gills in crayfish. Nub is expressed only in the posterior gill (labelled AP). (H) Summary of hypothetical relationships between insect tracheae and crustacean gills. Colour code is cyan for appendages/legs (expressing Dll in all arthropods), red for AP gills and insect wings (straddling the AP boundary, and expressing nub and vvl/trh), and green for A gills and insect tracheae (comprising anterior cells only, and expressing vvl and trh, but not nub).

 





© The Company of Biologists Ltd 2006