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First published online 16 June 2004
doi: 10.1242/dev.01201

Development 131, 3285-3294 (2004)
Published by The Company of Biologists 2004
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Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development

Tokiharu Takahashi1,2 and Peter W. H. Holland1,*

1 Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
2 Department of Hematology and Oncology, Graduate School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan

* Author for correspondence (e-mail: peter.holland{at}zoo.ox.ac.uk)

Accepted 1 April 2004

The ancestral chordate neural tube had a tripartite structure, comprising anterior, midbrain-hindbrain boundary (MHB) and posterior regions. The most anterior region encompasses both forebrain and midbrain in vertebrates. It is not clear when or how the distinction between these two functionally and developmentally distinct regions arose in evolution. Recently, we reported a mouse PRD-class homeobox gene, Dmbx1, expressed in the presumptive midbrain at early developmental stages, and the hindbrain at later stages, with exclusion from the MHB. This gene provides a route to investigate the evolution of midbrain development. We report the cloning, genomic structure, phylogeny and embryonic expression of Dmbx genes from amphioxus and from Ciona, representing the two most closely related lineages to the vertebrates. Our analyses show that Dmbx genes form a distinct, ancient, homeobox gene family, with highly conserved sequence and genomic organisation, albeit more divergent in Ciona. In amphioxus, no Dmbx expression is observed in the neural tube, supporting previous arguments that the MHB equivalent region has been secondarily modified in evolution. In Ciona, the CiDmbx gene is detected in neural cells caudal to Pax2/5/8-positive cells (MHB homologue), in the Hox-positive region, but, interestingly, not in any cells rostral to them. These results suggest that a midbrain homologue is missing in Ciona, and argue that midbrain development is a novelty that evolved specifically on the vertebrate lineage. We discuss the evolution of midbrain development in relation to the ancestry of the tripartite neural ground plan and the origin of the MHB organiser.

Key words: Dmbx1, AmphiDmbx, CiDmbx, Ciona, Chordate, MHB, Isthmus






© The Company of Biologists Ltd 2004