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Importance of SoxE in neural crest development and the evolution of the pharynx

Abstract

The neural crest, a defining character of vertebrates1, is of prime importance to their evolutionary origin2. To understand neural crest evolution, we explored molecular mechanisms underlying craniofacial development in the basal jawless vertebrate, sea lamprey (Petromyzon marinus), focusing on the SoxE (Sox8, Sox9 and Sox10) gene family. In jawed vertebrates, these are important transcriptional regulators of the neural crest3, and the loss of Sox9 causes abnormal craniofacial development4,5. Here we report that two lamprey SoxE genes are expressed in migrating neural crest and crest-derived prechondrocytes in posterior branchial arches, whereas a third paralogue is expressed later in the perichondrium and mandibular arch. Morpholino knock-down of SoxE1 reveals that it is essential for posterior branchial arch development, although the mandibular arch is unaffected. The results show that chondrogenic function of SoxE regulators can be traced to the lamprey–gnathostome common ancestor and indicate that lamprey SoxE genes might have undergone independent duplication to have distinct functions in mandibular versus caudal branchial arches. This work sheds light on the homology of vertebrate branchial arches and supports their common origin at the base of vertebrates.

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Figure 1: SoxE RNA transcripts in neural crest within branchial arches.
Figure 2: SoxE1 MO effects on pharyngeal development.

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Acknowledgements

We thank J. Langeland for providing embryonic cDNA libraries; D. Meulemans for SoxE oligonucleotide primer sequences, T. Sauka-Spengler for SoxE2 and SoxE3 library screens, R. Bergstedt and the staff at Hammond Bay Biological Station for facilities and technical assistance; R. Kusakabe for providing the LjMA2 DNA construct, and L. Trinh for assistance with confocal microscopy imaging techniques. This work was supported by a grant to M.B.F. from the National Aeronautics and Space Administration.

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Correspondence to David W. McCauley.

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PmSoxE1, PmSoxE2, PmSoxE3 and PmSoxF sequences are deposited in GenBank under accession numbers AY830453, DQ328983, DQ328984 and AY830454, respectively. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Methods, Supplementary Figures 1–4 and Supplementary Discussion. (PDF 361 kb)

Supplementary Movie 1

Quicktime Movie through a dorsal-to-ventral Z-series of confocal images illustrating SoxE1 RNA expression in a stage 25 embryo at different dorsoventral levels within developing branchial arches. Presumptive cartilage cells, shown in red, express SoxE1 in branchial arches. Rostrally (righthand side) pharyngeal endodermal outpockets contact ectoderm to form branchial arches and expression of SoxE1 in the rostralmost arch is in differentiating chondrocytes.. In the caudal region shown (lefthand side), endoderm does not contact ectoderm and SoxE1 expression is present in undifferentiated ectomesenchymal neural crest. Dorsally (start of movie), the caudal pharyngeal outpocketing nearly contacts the ectoderm to form a branchial arch. Ventrally (end of movie), the endodermal outpocket is shown at a greater distance from ectoderm than its dorsal position at the start of the movie. Lamprey autofluorescence shown in green. (MOV 1417 kb)

Supplementary Movie 2

Quicktime movie through a dorsal-to-ventral Z-series of confocal images illustrating SoxE2 RNA expression in a stage 25 embryo at different dorsoventral levels within branchial arches. SoxE2 RNA expression is present only in stacks of prechondrocytes within each arch. (MOV 420 kb)

Supplementary Movie 3

Quicktime movie through a dorsal-to-ventral Z-series of confocal images illustrating SoxE3 expression in a stage 25 embryo at different dorsoventral levels within a developing branchial arch. SoxE3 RNA is expressed in the perichondrial cells surrounding the chondrocytes, but is not present in the stacked chondrocytes within the branchial arch shown. (MOV 1945 kb)

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McCauley, D., Bronner-Fraser, M. Importance of SoxE in neural crest development and the evolution of the pharynx. Nature 441, 750–752 (2006). https://doi.org/10.1038/nature04691

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