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Lamprey snail highlights conserved and novel patterning roles in vertebrate embryos

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Abstract

snail genes mark presumptive mesoderm across bilaterian animals. In gnathostome vertebrates, snail genes are a multimember family that are also markers of premigratory neural crest (pnc) and some postmigratory neural crest derivatives in the pharyngeal arches. Previous studies of nonvertebrate chordates indicate that they have single snail genes that retain ancestral functions in mesoderm development and perhaps in specification of a pnc-like cell population. Lampreys are the most basal extant vertebrates, with well-defined developmental morphology. Here, we identify a single snail gene from the lamprey Petromyzon marinus that is the phylogenetic outgroup of all gnathostome snail genes. This single lamprey snail gene retains ancestral snail patterning domains present in nonvertebrate chordates. Lamprey snail is also expressed in tissues that are broadly equivalent to the combined sites of expression of all three gnathostome snail paralogy groups, excepting in embryonic tissues that are unique to gnathostomes. Importantly, while snail does not appear to demarcate an early neural crest population in lampreys as it does in gnathostomes, it may be involved in later neural crest development. Together, our results indicate that significant cis-regulatory innovation occurred in a single snail gene before the vertebrate radiation, and significant subfunctionalization occurred after snail gene duplications in the gnathostome lineages.

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Acknowledgments

We thank Roger Bergstedt and the staff of the Lake Huron Biological Station for their assistance in the rearing of lamprey embryos. This work was supported by NSF Award No. IBN-0110540 to JAL.

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Correspondence to James A. Langeland.

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Communicated by M. Hammerschmidt

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Rahimi, R.A., Allmond, J.J., Wagner, H. et al. Lamprey snail highlights conserved and novel patterning roles in vertebrate embryos. Dev Genes Evol 219, 31–36 (2009). https://doi.org/10.1007/s00427-008-0258-4

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  • DOI: https://doi.org/10.1007/s00427-008-0258-4

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