Drosophila cardiac tube organogenesis requires multiple phases of Hox activity.
The segmented Drosophila linear cardiac tube originates from two cell lineages that give rise to the anterior aorta (AA) and the posterior cardiac tube. The three Hox genes of the Bithorax Complex as well as Antennapedia (Antp) have been shown to be expressed in the posterior cardiac tube, while no Hox gene is expressed in the anterior aorta. We show that the cells of the whole tube adopt the anterior aorta identity in the complete absence of Hox function. Conversely, ectopic expression of Antp, Ultrabithorax (Ubx), or abdominal-A (abd-A) transformed the anterior aorta into posterior cardiac tube by all available criteria, indicating an equivalent early function in their ability to direct a posterior cardiac tube lineage. We further demonstrate that Hox genes act in a subsequent step during cardiac tube organogenesis, specifically on the differentiation of posterior cardiac tube myocytes. In addition, while some of these functions are fulfilled equally well by any one of the three Hox genes, some others are specific to a given Hox. Notably, the gene encoding the anion transporter Na+-Driven Anion Exchanger 1 behaves as a Hox differential transcriptional target and is activated by abd-A in the heart and repressed by Ubx in the posterior aorta. This analysis illustrates the mechanisms by which Hox genes can orchestrate organogenesis and, in particular, allows a clear uncoupling of the different phases of Hox activity in this process.
Perrin
Laurent
L
Laboratoire de Génétique et Physiologie du Développement, UMR 6545 CNRS-Université, IBDM-CNRS-Université de la Méditerranée, Marseille Cedex 09, 13288 France.
Monier
Bruno
B
Ponzielli
Romina
R
Astier
Martine
M
Semeriva
Michel
M
D000818:Animals; D051943:Antennapedia Homeodomain Protein; D017920:Antiporters / Q000235:genetics / Q000378:metabolism; D001011:Aorta / Q000196:embryology; D015415:Biomarkers; D002454:Cell Differentiation / Q000502:physiology; D019070:Cell Lineage; D004330:Drosophila / Q000196:embryology / Q000235:genetics; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004625:Embryo, Nonmammalian; D018507:Gene Expression Regulation, Developmental; D006321:Heart / Q000196:embryology*; D018398:Homeodomain Proteins / Q000235:genetics / Q000378:metabolism*; D009154:Mutation; D009206:Myocardium / Q000166:cytology; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism; D038081:Organogenesis; D039904:Pluripotent Stem Cells / Q000502:physiology; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
C062393:Abd-B proteins, Drosophila; D051943:Antennapedia Homeodomain Protein; D017920:Antiporters; C497974:Antp protein, Drosophila; D015415:Biomarkers; D029721:Drosophila Proteins; D018398:Homeodomain Proteins; C491441:NDAE1 protein, Drosophila; D009687:Nuclear Proteins; C059627:Scr protein, Drosophila; D014157:Transcription Factors; C066177:Ubx protein, Drosophila; C066591:abd-A protein, Drosophila