Gene regulatory evolution and the origin of macroevolutionary novelties: insights from the neural crest

Eric Van Otterloo; Robert A Cornell; Daniel Meulemans Medeiros; Aaron T Garnett

doi:10.1002/dvg.22403

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Gene regulatory evolution and the origin of macroevolutionary novelties: insights from the neural crest

Journal article

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Gene regulatory evolution and the origin of macroevolutionary novelties: insights from the neural crest

Eric Van Otterloo, Robert A Cornell, Daniel Meulemans Medeiros and Aaron T Garnett

Genesis (New York, N.Y. : 2000), Vol.51(7), pp.457-470

07/2013

DOI: 10.1002/dvg.22403

PMCID: PMC4249638

PMID: 23712931

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Abstract

The appearance of novel anatomic structures during evolution is driven by changes to the networks of transcription factors, signaling pathways, and downstream effector genes controlling development. The nature of the changes to these developmental gene regulatory networks (GRNs) is poorly understood. A striking test case is the evolution of the GRN controlling development of the neural crest (NC). NC cells emerge from the neural plate border (NPB) and contribute to multiple adult structures. While all chordates have a NPB, only in vertebrates do NPB cells express all the genes constituting the neural crest GRN (NC-GRN). Interestingly, invertebrate chordates express orthologs of NC-GRN components in other tissues, revealing that during vertebrate evolution new regulatory connections emerged between transcription factors primitively expressed in the NPB and genes primitively expressed in other tissues. Such interactions could have evolved by two mechanisms. First, transcription factors primitively expressed in the NPB may have evolved new DNA and/or cofactor binding properties (protein neofunctionalization). Alternately, cis-regulatory elements driving NPB expression may have evolved near genes primitively expressed in other tissues (cis-regulatory neofunctionalization). Here we discuss how gene duplication can, in principle, promote either form of neofunctionalization. We review recent published examples of interspecies gene-swap, or regulatory-element-swap, experiments that test both models. Such experiments have yielded little evidence to support the importance of protein neofunctionalization in the emergence of the NC-GRN, but do support the importance of novel cis-regulatory elements in this process. The NC-GRN is an excellent model for the study of gene regulatory and macroevolutionary innovation.

Chordata - embryology

Chordata - genetics

Gene Duplication

Neural Crest - growth & development

Gene Dosage

Neural Plate - growth & development

Phylogeny

Gene Regulatory Networks

Biological Evolution

Neural Crest - physiology

Animals

Gene Expression Regulation, Developmental

Neural Plate - physiology

Evolution, Molecular

Details

Title: Subtitle: Gene regulatory evolution and the origin of macroevolutionary novelties: insights from the neural crest
Creators: Eric Van Otterloo - Department of Anatomy and Cell Biology, University of Iowa, Iowa City, IA, USA
Robert A Cornell
Daniel Meulemans Medeiros
Aaron T Garnett
Resource Type: Journal article
Publication Details: Genesis (New York, N.Y. : 2000), Vol.51(7), pp.457-470
DOI: 10.1002/dvg.22403
PMID: 23712931
PMCID: PMC4249638
NLM abbreviation: Genesis
ISSN: 1526-954X
eISSN: 1526-968X
Publisher: United States
Grant note: 1R03DE019804 / NIDCR NIH HHS R03 DE019804 / NIDCR NIH HHS
Language: English
Date published: 07/2013
Academic Unit: Anatomy and Cell Biology; Craniofacial Anomalies Research Center; Dental Research; Periodontics
Record Identifier: 9984025351902771

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