Expression of FoxC, FoxF, FoxL1, and FoxQ1 genes in the dogfish <i>Scyliorhinus canicula</i> defines ancient and derived roles for fox genes in vertebrate development

Wotton, Karl R.; Mazet, Françoise; Shimeld, Sebastian M.

doi:10.1002/dvdy.21553

Cited by 32 publications

(43 citation statements)

References 79 publications

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“…Interestingly, expression studies of FoxC paralogues in the shark Scyliorhinus canicula report that FoxC1 is expressed in pharyngeal arch mesenchyme, while FoxC2 is expressed exclusively in pharyngeal endoderm-a site of expression that has not been described in any other vertebrate to date [48]. While Wotton et al [48] consider this endodermal expression of FoxC2 to be a derived condition of chondrichthyans, our findings hint at a possible primitive role for FoxC expression in deuterostome pharyngeal endoderm. .…”

Section: Discussionmentioning

confidence: 47%

A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network

2011

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Hemichordate worms possess ciliated gills on their trunk, and the homology of these structures with the pharyngeal gill slits of chordates has long been a topic of debate in the fields of evolutionary biology and comparative anatomy. Here, we show conservation of transcription factor expression between the developing pharyngeal gill pores of the hemichordate Saccoglossus kowalevskii and the pharyngeal gill slit precursors (i.e. pharyngeal endodermal outpockets) of vertebrates. Transcription factors that are expressed in the pharyngeal endoderm, ectoderm and mesenchyme of vertebrates are expressed exclusively in the pharyngeal endoderm of S. kowalevskii. The pharyngeal arches and tongue bars of S. kowalevskii lack Tbx1-expressing mesoderm, and are supported solely by an acellular collagenous endoskeleton and by compartments of the trunk coelom. Our findings suggest that hemichordate and vertebrate gills are homologous as simple endodermal outpockets from the foregut, and that much vertebrate pharyngeal complexity arose coincident with the incorporation of cranial paraxial mesoderm and neural crest-derived mesenchyme within pharyngeal arches along the chordate and vertebrate stems, respectively.

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Section: Discussionmentioning

confidence: 47%

A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network

2011

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“…We hereafter refer to these genes collectively as the clustered Fox genes, although this is not to suggest that the genes are clustered in all lineages, only that we can infer they were primitively clustered. These studies show that the two vertebrate Fox clusters arose by means of en bloc duplication from a single cluster and that this duplication occurred after the divergence of vertebrates and amphioxus, but before the radiation of the jawed vertebrates (Wotton et al, 2008a). One further vertebrate lineage diverged between these nodes; the agnathans, whose extant members are the lampreys and hagfish (Delsuc et al, 2006;Dumeril, 1806;Furlong and Holland, 2002;Kuraku et al, 1999;Romer, 1966).…”

Section: Evolution Of the Clustered Fox Genesmentioning

confidence: 91%

Analysis of lamprey clustered Fox genes: Insight into Fox gene evolution and expression in vertebrates

Wotton

Shimeld

2011

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“…Hox gene clustering is functionally significant, related to spatiotemporal expression and this is a constraining factor on genomic organization (Tschopp et al 2009). Other clustered genes often show features suggestive of constraint on their organization such as shared or coordinated expression patterns (Houweling et al 2001;Jagla et al 2001;Mazet et al 2006;Wotton et al 2008a). However, features corresponding to the Hox global control regions or progressive changes in chromatin state have, so far, generally not been identified in other gene clusters and identifying the genomic features that keep different clustered genes closely linked represents a considerable challenge to the field.…”

Section: Introductionmentioning

confidence: 97%

Conservation of gene linkage in dispersed vertebrate NK homeobox clusters

et al. 2009

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Nk homeobox genes are important regulators of many different developmental processes including muscle, heart, central nervous system and sensory organ development. They are thought to have arisen as part of the ANTP megacluster, which also gave rise to Hox and ParaHox genes, and at least some NK genes remain tightly linked in all animals examined so far. The protostome-deuterostome ancestor probably contained a cluster of nine Nk genes: (Msx)-(Nk4/tinman)-(Nk3/bagpipe)-(Lbx/ladybird)-(Tlx/c15)-(Nk7)-(Nk6/hgtx)-(Nk1/slouch)-(Nk5/Hmx). Of these genes, only NKX2.6-NKX3.1, LBX1-TLX1 and LBX2-TLX2 remain tightly linked in humans. However, it is currently unclear whether this is unique to the human genome as we do not know which of these Nk genes are clustered in other vertebrates. This makes it difficult to assess whether the remaining linkages are due to selective pressures or because chance rearrangements have "missed" certain genes. In this paper, we identify all of the paralogs of these ancestrally clustered NK genes in several distinct vertebrates. We demonstrate that tight linkages of Lbx1-Tlx1, Lbx2-Tlx2 and Nkx3.1-Nkx2.6 have been widely maintained in both the ray-finned and lobe-finned fish lineages. Moreover, the recently duplicated Hmx2-Hmx3 genes are also tightly linked. Finally, we show that Lbx1-Tlx1 and Hmx2-Hmx3 are flanked by highly conserved noncoding elements, suggesting that shared regulatory regions may have resulted in evolutionary pressure to maintain these linkages. Consistent with this, these pairs of genes have overlapping expression domains. In contrast, Lbx2-Tlx2 and Nkx3.1-Nkx2.6, which do not seem to be coexpressed, are also not associated with conserved noncoding sequences, suggesting that an alternative mechanism may be responsible for the continued clustering of these genes.

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Expression of FoxC, FoxF, FoxL1, and FoxQ1 genes in the dogfish Scyliorhinus canicula defines ancient and derived roles for fox genes in vertebrate development

Cited by 32 publications

References 79 publications

A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network

A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network

Analysis of lamprey clustered Fox genes: Insight into Fox gene evolution and expression in vertebrates

Conservation of gene linkage in dispersed vertebrate NK homeobox clusters

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