Developmental expression of the amphioxus Tbx1/10 gene illuminates the evolution of vertebrate branchial arches and sclerotome
- 328 Downloads
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.
KeywordsT-box Tbx1 Tbx10 Amphioxus Sclerotome
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analyses, Mike Veith for instruction in cutting plastic sections, and Paris Ataliotis for providing access to his unpublished Xenopus Tbx1 sequence.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.
- Ataliotis P, Latinkic B, Mohun TJ, Scambler PJ (2001) Analysis of Tbx1 function in Xenopus laevis. Dev Biol 235:245Google Scholar
- Hall BK (1994) Homology: the hierachical basis of comparative biology. Academic, San DiegoGoogle Scholar
- Holland ND, Holland LZ (1993) Embryos and larvae of invertebrate deuterostomes. In Stern CD, Holland PWH (eds) Essential developmental biology: a practical approach. IRL Press, Oxford, pp 21–32Google Scholar
- Holland LZ, Holland PWH, Holland ND (1996) Revealing homologies between body parts of distantly related animals by in situ hybridization to developmental genes: amphioxus versus vertebrates. In: Ferraris JD, Palumbi SR (eds) Molecular zoology: advances, strategies, and protocols. Wiley-Liss, New York, pp 267–282, 473–483Google Scholar
- Horton AC, Mahadevan NR, Ruvinsky I, Gibson-Brown JJ (2003) Phylogenetic analyses alone are insufficient to determine whether whole-genome duplication(s) occurred during early vertebrate evolution. J Exp Zool Part B Mol Dev Evol 299:41–53Google Scholar
- Merscher S, Funke B, Epstein JA, Heyer J, Peuch A, Lu MM, Xavier RJ, Demay MB, Russell RG, Factor S, Tokooya K, Jore B St, Lopez M, Pandita RK, Lia M, Carrion M, Xu H, Schorle H, Kobler JB, Scambler P, Wynshaw-Boris A, Skoultchi AI, Morrow BE, Kucherlapati R (2001) TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell 104:619–629CrossRefPubMedGoogle Scholar
- Ohno S (1970) Evolution by gene duplication. Springer, Berlin Heidelberg New YorkGoogle Scholar
- Swofford DL (2001) PAUP* beta 5: phylogenetic analysis using parsimony (and other methods). Sinauer, Sunderland, Mass.Google Scholar