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doi: 10.1242/10.1242/dev.00438


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Development 130, 2365-2373 (2003)
Copyright © 2003 The Company of Biologists Limited

An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila

Frank Hirth1,*,{dagger}, Lars Kammermeier1,*, Erich Frei2, Uwe Walldorf3, Markus Noll2 and Heinrich Reichert1

1 Institute of Zoology, Biozentrum/Pharmazentrum, University of Basel, Klingelbergstrasse 50, CH-4056 Basel, Switzerland
2 Institute for Molecular Biology, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
3 Department of Anatomy and Cell Biology, University of Saarland, Building 61, D-66421 Homburg/Saar, Germany

{dagger} Author for correspondence (e-mail: frank.hirth{at}unibas.ch)

Accepted 10 February 2003

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.

Key words: Brain development, Brain evolution, Midbrain/hindbrain boundary, Otx, Hox, Pax, Drosophila melanogaster


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