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Developmental expression of the amphioxus Tbx1/10 gene illuminates the evolution of vertebrate branchial arches and sclerotome

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Abstract

We have isolated an amphioxus T-box gene that is orthologous to the two vertebrate genes, Tbx1 and Tbx10, and examined its expression pattern during embryonic and early larval development. AmphiTbx1/10 is first expressed in branchial arch endoderm and mesoderm of developing neurulae, and in a bilateral, segmented pattern in the ventral half of newly formed somites. Branchial expression is restricted to the first three branchial arches, and disappears completely by 4 days post fertilization. Ventral somitic expression is restricted to the first 10–12 somites, and is not observed in early larvae except in the most ventral mesoderm of the first three branchial arches. No expression can be detected by 4 days post fertilization. Integrating functional, phylogenetic and expression data from amphioxus and a variety of vertebrate model organisms, we have reconstructed the early evolutionary history of the Tbx1/10 subfamily of genes within the chordate lineage. We conclude that Tbx1/10-mediated branchial arch endoderm and mesoderm patterning functions predated the origin of neural crest, and that ventral somite specification functions predated the origin of vertebrate sclerotome, but that Tbx1 was later co-opted during the evolution of developmental programs regulating branchial neural crest and sclerotome migration.

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Acknowledgements

We wish to thank Nick and Linda Holland for instruction in the collection of amphioxus embryos and whole-mount in situ hybridization, Jim Langeland for the amphioxus cDNA library, John Lawrence and Skip Pierce for providing laboratory space at the University of South Florida, Amy Horton and Ilya Ruvinsky for advice on phylogenetic analyses, Mike Veith for instruction in cutting plastic sections, and Paris Ataliotis for providing access to his unpublished Xenopus Tbx1 sequence. Finally, we are most grateful to Lee Silver, in whose laboratory at Princeton these studies were initiated, for his generous support. This work was supported by NIH grant HD-20275 to Lee M. Silver, a Beckman Scholar award to N.M., a Development Traveling Fellowship from The Company of Biologists, and departmental support from Washington University to J.J.G.-B.

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Correspondence to Jeremy J. Gibson-Brown.

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Edited by M. Akam

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Mahadevan, N.R., Horton, A.C. & Gibson-Brown, J.J. Developmental expression of the amphioxus Tbx1/10 gene illuminates the evolution of vertebrate branchial arches and sclerotome. Dev Genes Evol 214, 559–566 (2004). https://doi.org/10.1007/s00427-004-0433-1

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