Central role of gene cooption in neural crest evolution

Meulemans, Daniel; Bronner‐Fraser, Marianne

doi:10.1002/jez.b.21047

Cited by 60 publications

(56 citation statements)

References 32 publications

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“…(2,91,93) However, most neural crest specifier genes (AP2, FoxD, Id, SoxE, Twist) were only recruited to this region in vertebrates associated with the evolution of a population of multipotential migratory cells, i.e. a true neural crest.…”

Section: Problems and Paradigmsmentioning

confidence: 99%

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Do vertebrate neural crest and cranial placodes have a common evolutionary origin?

Schlosser

2008

BioEssays

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Two embryonic tissues-the neural crest and the cranial placodes-give rise to most evolutionary novelties of the vertebrate head. These two tissues develop similarly in several respects: they originate from ectoderm at the neural plate border, give rise to migratory cells and develop into multiple cell fates including sensory neurons. These similarities, and the joint appearance of both tissues in the vertebrate lineage, may point to a common evolutionary origin of neural crest and placodes from a specialized population of neural plate border cells. However, a review of the developmental mechanisms underlying the induction, specification, migration and cytodifferentiation of neural crest and placodes reveals fundamental differences between the tissues. Taken together with insights from recent studies in tunicates and amphioxus, this suggests that neural crest and placodes have an independent evolutionary origin and that they evolved from the neural and non-neural side of the neural plate border, respectively.

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Section: Problems and Paradigmsmentioning

confidence: 99%

“…(2,5,21,91 -93) Homologues of the ''neural plate border specifiers'' Zic, Msx, Pax3/7 and of Snail are expressed on the neural side of the neural plate border in amphioxus and some tunicates. (2,91,93) In tunicates but not amphioxus, Msx and Pax3/7…”

Section: Problems and Paradigmsmentioning

confidence: 99%

Do vertebrate neural crest and cranial placodes have a common evolutionary origin?

Schlosser

2008

BioEssays

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“…Importantly, at least some regulatory interactions within the NC GRN must be evolutionarily novel because many of the transcription factors contributing to the NC GRN were recruited to the neural-plate border from other tissues (Meulemans and Bronner-Fraser, 2005). The evolution of novel regulatory interactions can result from mutations causing 'protein neofunctionalization', or those causing 'regulatory neofunctionalization'.…”

Section: Introductionmentioning

confidence: 99%

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

Otterloo

Garnett³

et al. 2012

Development

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SUMMARYGene 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 neofunctionalization 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.

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“…For instance, in the most basal chordate, the cephalochordate amphioxus, most neural plate border specifiers are found in the neural plate border whereas most neural crest specifiers, with the exception of Snail that is found in the neural tube, are expressed in the underlying mesoderm (Meulemans and Bronner-Fraser, 2005;Meulemans and Bronner-Fraser, 2007;Baker, 2008). It is possible that a group of genes forming the 'neural crest specifier module' was recruited by some cells in the neuroepithelial domain (future neural crest), whereas SoxE genes were co-opted simultaneously by presumptive neural crest and otic placode cells found in the same domain.…”

Section: Research Articlementioning

confidence: 99%

A Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs

2011

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SUMMARYThe otic placode, a specialized region of ectoderm, gives rise to components of the inner ear and shares many characteristics with the neural crest, including expression of the key transcription factor Sox10. Here, we show that in avian embryos, a highly conserved cranial neural crest enhancer, Sox10E2, also controls the onset of Sox10 expression in the otic placode. Interestingly, we show that different combinations of paralogous transcription factors (Sox8, Pea3 and cMyb versus Sox9, Ets1 and cMyb) are required to mediate Sox10E2 activity in the ear and neural crest, respectively. Mutating their binding motifs within Sox10E2 greatly reduces enhancer activity in the ear. Moreover, simultaneous knockdown of Sox8, Pea3 and cMyb eliminates not only the enhancer-driven reporter expression, but also the onset of endogenous Sox10 expression in the ear. Rescue experiments confirm that the specific combination of Myb together with Sox8 and Pea3 is responsible for the onset of Sox10 expression in the otic placode, as opposed to Myb plus Sox9 and Ets1 for neural crest Sox10 expression. Whereas SUMOylation of Sox8 is not required for the initial onset of Sox10 expression, it is necessary for later otic vesicle formation. This new role of Sox8, Pea3 and cMyb in controlling Sox10 expression via a common otic/neural crest enhancer suggests an evolutionarily conserved function for the combination of paralogous transcription factors in these tissues of distinct embryological origin. KEY WORDS: Ear, Cis-regulation, Sox10, ChickA Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs

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Central role of gene cooption in neural crest evolution

Cited by 60 publications

References 32 publications

Do vertebrate neural crest and cranial placodes have a common evolutionary origin?

Do vertebrate neural crest and cranial placodes have a common evolutionary origin?

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

A Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs

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