Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development.

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...

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Main Authors: Takahashi, T, Holland, P
Format: Journal article
Language:English
Published: 2004
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author Takahashi, T
Holland, P
author_facet Takahashi, T
Holland, P
author_sort Takahashi, T
collection OXFORD
description 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.
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spelling oxford-uuid:4d55e2a8-522f-424b-8bad-4078d4427e5b2022-03-26T15:54:56ZAmphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development.Journal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:4d55e2a8-522f-424b-8bad-4078d4427e5bEnglishSymplectic Elements at Oxford2004Takahashi, THolland, PThe 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.
spellingShingle Takahashi, T
Holland, P
Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development.
title Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development.
title_full Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development.
title_fullStr Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development.
title_full_unstemmed Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development.
title_short Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development.
title_sort amphioxus and ascidian dmbx homeobox genes give clues to the vertebrate origins of midbrain development
work_keys_str_mv AT takahashit amphioxusandascidiandmbxhomeoboxgenesgivecluestothevertebrateoriginsofmidbraindevelopment
AT hollandp amphioxusandascidiandmbxhomeoboxgenesgivecluestothevertebrateoriginsofmidbraindevelopment