An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila.
Studies on expression and function of key developmental control genes suggest that the embryonic vertebrate brain has a tripartite ground plan that consists of a forebrain/midbrain, a hindbrain and an intervening midbrain/hindbrain boundary region, which are characterized by the specific expression of the Otx, Hox and Pax2/5/8 genes, respectively. We show that the embryonic brain of the fruitfly Drosophila melanogaster expresses all three sets of homologous genes in a similar tripartite pattern. Thus, a Pax2/5/8 expression domain is located at the interface of brain-specific otd/Otx2 and unpg/Gbx2 expression domains anterior to Hox expression regions. We identify this territory as the deutocerebral/tritocerebral boundary region in the embryonic Drosophila brain. Mutational inactivation of otd/Otx2 and unpg/Gbx2 result in the loss or misplacement of the brain-specific expression domains of Pax2/5/8 and Hox genes. In addition, otd/Otx2 and unpg/Gbx2 appear to negatively regulate each other at the interface of their brain-specific expression domains. Our studies demonstrate that the deutocerebral/tritocerebral boundary region in the embryonic Drosophila brain displays developmental genetic features similar to those observed for the midbrain/hindbrain boundary region in vertebrate brain development. This suggests that a tripartite organization of the embryonic brain was already established in the last common urbilaterian ancestor of protostomes and deuterostomes.
Hirth
Frank
F
Institute of Zoology, Biozentrum/Pharmazentrum, University of Basel, Klingelbergstrasse 50, CH-4056 Basel, Switzerland. frank.hirth@unibas.ch
Kammermeier
Lars
L
Frei
Erich
E
Walldorf
Uwe
U
Noll
Markus
M
Reichert
Heinrich
H
D000818:Animals; D030801:Animals, Genetically Modified; D001921:Brain / Q000196:embryology*; D004268:DNA-Binding Proteins / Q000235:genetics; D029721:Drosophila Proteins / Q000235:genetics; D004331:Drosophila melanogaster / Q000196:embryology* / Q000235:genetics*; D018507:Gene Expression Regulation, Developmental; D005801:Genes, Homeobox; D017344:Genes, Insect; D018398:Homeodomain Proteins / Q000235:genetics; D009154:Mutation; D009419:Nerve Tissue Proteins / Q000235:genetics; D051762:PAX2 Transcription Factor; D051761:Paired Box Transcription Factors; D013045:Species Specificity; D014157:Transcription Factors / Q000235:genetics; D014714:Vertebrates / Q000196:embryology / Q000235:genetics
D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D018398:Homeodomain Proteins; D009419:Nerve Tissue Proteins; D051762:PAX2 Transcription Factor; D051761:Paired Box Transcription Factors; C073863:Poxn protein, Drosophila; D014157:Transcription Factors; C093053:oc protein, Drosophila; C098131:unpg protein, Drosophila