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Published August 23, 2011 | Published + Supplemental Material
Journal Article Open

Transphyletic conservation of developmental regulatory state in animal evolution


Specific regulatory states, i.e., sets of expressed transcription factors, define the gene expression capabilities of cells in animal development. Here we explore the functional significance of an unprecedented example of regulatory state conservation from the cnidarian Nematostella to Drosophila, sea urchin, fish, and mammals. Our probe is a deeply conserved cis-regulatory DNA module of the SRY-box B2 (soxB2), recognizable at the sequence level across many phyla. Transphyletic cis-regulatory DNA transfer experiments reveal that the plesiomorphic control function of this module may have been to respond to a regulatory state associated with neuronal differentiation. By introducing expression constructs driven by this module from any phyletic source into the genomes of diverse developing animals, we discover that the regulatory state to which it responds is used at different levels of the neurogenic developmental process, including patterning and development of the vertebrate forebrain and neurogenesis in the Drosophila optic lobe and brain. The regulatory state recognized by the conserved DNA sequence may have been redeployed to different levels of the developmental regulatory program during evolution of complex central nervous systems.

Additional Information

© 2011 National Academy of Sciences. Contributed by Eric H. Davidson, June 8, 2011 (sent for review April 19, 2011). Published online before print August 15, 2011. We thank Billie J. Swalla, Paola Oliveri, Pedro Martínez, and F. Rentzsch for providing genomic DNAs and José Luis Ferrán for helpful comments. We also thank A. Cameron for technical assistance with sea urchins and J. Barsi from the E.H.D. laboratory for protocols. F.G. was supported by National Science Foundation Grant IOS-0641398 (to E.H.D.) and by the Camilla Chandler Frost Fellowship. I.S.P. was supported by National Institutes of Health Grant HD037105 (to E.H.D.). M.I., I.M., and J.G.-F. were funded by Grants BFU2005-00252 and BMC2008-03776 from the Spanish Ministry of Science and Innovation. M.I. and I.M. hold Formación de Personal Investigador and Formación de Personal Universitario grants, respectively. J.G.-F. was funded by Institució Catalana de Recerca i Estudis Avançats Academia, Generalitat de Catalunya, Spain. F.C. was supported by Grants BFU2009-07044 from the Spanish Ministry of Science and Innovation and CVI 2658 (Junta de Andalucía); and J.L.G.-S. was supported by Grants BFU2010-14839, CSD2007-00008 (Ministerio de Ciencia e Innovación), and Proyecto de Excelencia CVI 3488 (Junta de Andalucía). Author contributions: J.L.R., I.M., M.I., I.S.P., C.L., F.C., E.H.D., J.G.-F., and J.L.G.-S. designed research; J.L.R., I.M., M.I., F.G., C.L., S.D., and J.L.G.-S. performed research; and J.L.R., I.M., M.I., I.S.P., F.C., E.H.D., J.G.-F., and J.L.G.-S. wrote the paper.

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Published - 14186.full.pdf

Published - LuisRoyo2011p15694P_Natl_Acad_Sci_Usa.pdf

Supplemental Material - pnas.201109037SI.pdf


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