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Protochordate Zic genes define primitive somite compartments and highlight molecular changes underlying neural crest evolution

Protochordate Zic genes define primitive somite compartments and highlight molecular changes underlying neural crest evolution
Protochordate Zic genes define primitive somite compartments and highlight molecular changes underlying neural crest evolution
The vertebrate Zic gene family encodes C2H2 zinc finger transcription factors closely related to the Gli proteins. Zic genes are expressed in multiple areas of developing vertebrate embryos, including the dorsal neural tube where they act as potent neural crest inducers. Here we describe the characterization of a Zic ortholog from the amphioxus Branchiostoma floridae and further describe the expression of a Zic ortholog from the ascidian Ciona intestinalis. Molecular phylogenetic analysis and sequence comparisons suggest the gene duplications that formed the vertebrate Zic family were specific to the vertebrate lineage. In Ciona maternal CiZic/Ci-macho1 transcripts are localized during cleavage stages by asymmetric cell division, whereas zygotic expression by neural plate cells commences during neurulation. The amphioxus Zic ortholog AmphiZic is expressed in dorsal mesoderm and ectoderm during gastrulation, before being eliminated first from midline cells and then from all neurectoderm during neurulation. After neurulation, expression is reactivated in the dorsal neural tube and dorsolateral somite. Comparison of CiZic and AmphiZic expression with vertebrate Zic expression leads to two main conclusions. First, Zic expression allows us to define homologous compartments between vertebrate and amphioxus somites, showing primitive subdivision of vertebrate segmented mesoderm. Second, we show that neural Zic expression is a chordate synapomorphy, whereas the precise pattern of neural expression has evolved differently on the different chordate lineages. Based on these observations we suggest that a change in Zic regulation, specifically the evolution of a dorsal neural expression domain in vertebrate neurulae, was an important step in the evolution of the neural crest.
1520-541X
136-144
Gostling, Neil J.
4840aa40-cb6c-4112-a0b9-694a869523fc
Shimeld, Sebastian M.
ed6e18a4-73d5-4d51-aef2-018543e98e03
Gostling, Neil J.
4840aa40-cb6c-4112-a0b9-694a869523fc
Shimeld, Sebastian M.
ed6e18a4-73d5-4d51-aef2-018543e98e03

Gostling, Neil J. and Shimeld, Sebastian M. (2003) Protochordate Zic genes define primitive somite compartments and highlight molecular changes underlying neural crest evolution. Evolution & Development, 5 (2), 136-144. (doi:10.1046/j.1525-142X.2003.03020.x).

Record type: Article

Abstract

The vertebrate Zic gene family encodes C2H2 zinc finger transcription factors closely related to the Gli proteins. Zic genes are expressed in multiple areas of developing vertebrate embryos, including the dorsal neural tube where they act as potent neural crest inducers. Here we describe the characterization of a Zic ortholog from the amphioxus Branchiostoma floridae and further describe the expression of a Zic ortholog from the ascidian Ciona intestinalis. Molecular phylogenetic analysis and sequence comparisons suggest the gene duplications that formed the vertebrate Zic family were specific to the vertebrate lineage. In Ciona maternal CiZic/Ci-macho1 transcripts are localized during cleavage stages by asymmetric cell division, whereas zygotic expression by neural plate cells commences during neurulation. The amphioxus Zic ortholog AmphiZic is expressed in dorsal mesoderm and ectoderm during gastrulation, before being eliminated first from midline cells and then from all neurectoderm during neurulation. After neurulation, expression is reactivated in the dorsal neural tube and dorsolateral somite. Comparison of CiZic and AmphiZic expression with vertebrate Zic expression leads to two main conclusions. First, Zic expression allows us to define homologous compartments between vertebrate and amphioxus somites, showing primitive subdivision of vertebrate segmented mesoderm. Second, we show that neural Zic expression is a chordate synapomorphy, whereas the precise pattern of neural expression has evolved differently on the different chordate lineages. Based on these observations we suggest that a change in Zic regulation, specifically the evolution of a dorsal neural expression domain in vertebrate neurulae, was an important step in the evolution of the neural crest.

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Published date: March 2003
Organisations: Centre for Biological Sciences

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Local EPrints ID: 385766
URI: http://eprints.soton.ac.uk/id/eprint/385766
ISSN: 1520-541X
PURE UUID: bf30b70f-3133-4a1a-b168-2e2882282c96
ORCID for Neil J. Gostling: ORCID iD orcid.org/0000-0002-5960-7769

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Date deposited: 22 Jan 2016 10:18
Last modified: 18 Aug 2020 01:41

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