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Transphyletic conservation of developmental regulatory state in animal evolution

Royo, José Luis and Maeso, Ignacio and Irimia, Manuel and Gao, Feng and Peter, Isabelle S. and Lopes, Carla S. and D'Aniello, Salvatore and Casares, Fernando and Davidson, Eric H. and Garcia-Fernández, Jordi and Gómez-Skarmeta, José Luis (2011) Transphyletic conservation of developmental regulatory state in animal evolution. Proceedings of the National Academy of Sciences of the United States of America, 108 (34). pp. 14186-14191. ISSN 0027-8424. PMCID PMC3161536. https://resolver.caltech.edu/CaltechAUTHORS:20110912-113932797

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Abstract

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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1109037108 DOIArticle
http://www.pnas.org/content/108/34/14186PublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3161536/PubMed CentralArticle
http://www.pnas.org/content/108/34/14186/suppl/DCSupplementalPublisherSupporting Information
ORCID:
AuthorORCID
Peter, Isabelle S.0000-0003-3685-3147
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.
Funders:
Funding AgencyGrant Number
NSFIOS-0641398
Camilla Chandler Frost FellowshipUNSPECIFIED
NIHHD037105
Ministerio de Ciencia e Innovación (MICINN)BFU2005-00252
Ministerio de Ciencia e Innovación (MICINN)BMC2008-03776
Formación de Personal InvestigadorUNSPECIFIED
Formación de Personal UniversitarioUNSPECIFIED
Institució Catalana de Recerca i Estudis Avançats Academia, Generalitat de Catalunya, SpainUNSPECIFIED
Ministerio de Ciencia e Innovación (MICINN)BFU2009-07044
Junta de AndalucíaCVI 2658
Ministerio de Ciencia e Innovación (MICINN)BFU2010-14839
Ministerio de Ciencia e Innovación (MICINN)CSD2007-00008
Proyecto de Excelencia, Junta de AndalucíaCVI 3488
Subject Keywords:sequence conservation; evolution of development; transgenesis; enhancer; sox21
Issue or Number:34
PubMed Central ID:PMC3161536
Record Number:CaltechAUTHORS:20110912-113932797
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20110912-113932797
Official Citation:José Luis Royo, Ignacio Maeso, Manuel Irimia, Feng Gao, Isabelle S. Peter, Carla S. Lopes, Salvatore D'Aniello, Fernando Casares, Eric H. Davidson, Jordi Garcia-Fernández, and José Luis Gómez-Skarmeta Transphyletic conservation of developmental regulatory state in animal evolution PNAS 2011 108 (34) 14186-14191; published ahead of print August 15, 2011, doi:10.1073/pnas.1109037108
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:25298
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:12 Sep 2011 22:48
Last Modified:03 Oct 2019 03:04

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