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Novel Tfap2-mediated control of soxE expression facilitated the evolutionary emergence of the neural crest
Journal article   Open access   Peer reviewed

Novel Tfap2-mediated control of soxE expression facilitated the evolutionary emergence of the neural crest

Eric Van Otterloo, Wei Li, Aaron Garnett, Maria Cattell, Daniel Meulemans Medeiros and Robert A Cornell
Development (Cambridge), Vol.139(4), pp.720-730
02/2012
DOI: 10.1242/dev.071308
PMCID: PMC3265060
PMID: 22241841
url
https://doi.org/10.1242/dev.071308View
Published (Version of record) Open Access

Abstract

Gene duplication has been proposed to drive the evolution of novel morphologies. After gene duplication, it is unclear whether changes in the resulting paralogs' coding-regions, or in their cis-regulatory elements, contribute most significantly to the assembly of novel gene regulatory networks. The Transcription Factor Activator Protein 2 (Tfap2) was duplicated in the chordate lineage and is essential for development of the neural crest, a tissue that emerged with vertebrates. Using a tfap2-depleted zebrafish background, we test the ability of available gnathostome, agnathan, cephalochordate and insect tfap2 paralogs to drive neural crest development. With the exception of tfap2d (lamprey and zebrafish), all are able to do so. Together with expression analyses, these results indicate that sub-functionalization has occurred among Tfap2 paralogs, but that neo-functionalization of the Tfap2 protein did not drive the emergence of the neural crest. We investigate whether acquisition of novel target genes for Tfap2 might have done so. We show that in neural crest cells Tfap2 directly activates expression of sox10, which encodes a transcription factor essential for neural crest development. The appearance of this regulatory interaction is likely to have coincided with that of the neural crest, because AP2 and SoxE are not co-expressed in amphioxus, and because neural crest enhancers are not detected proximal to amphioxus soxE. We find that sox10 has limited ability to restore the neural crest in Tfap2-deficient embryos. Together, these results show that mutations resulting in novel Tfap2-mediated regulation of sox10 and other targets contributed to the evolution of the neural crest.
Chordata - genetics Drosophila melanogaster - embryology Zebrafish - anatomy & histology Humans Phylogeny Zebrafish - embryology Drosophila melanogaster - genetics Activating Transcription Factor 2 - genetics Protein Isoforms - metabolism Gene Expression Regulation, Developmental Lampreys - anatomy & histology Drosophila melanogaster - anatomy & histology Chordata - embryology Neural Crest - cytology Lampreys - embryology Chordata - anatomy & histology SOXE Transcription Factors - metabolism Embryonic Induction Activating Transcription Factor 2 - metabolism Zebrafish - genetics Lampreys - genetics Biological Evolution Neural Crest - physiology Animals Enhancer Elements, Genetic Chordata - classification Protein Isoforms - genetics SOXE Transcription Factors - genetics

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