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.................................................................Conservation and elaboration of Hox gene regulation during evolution of the vertebrate head
Miguel Manzanares*, Hiroshi Wadak, Nobue Itasaki*, Paul A. Trainor*, Robb Krumlauf* & Peter W. H. Hollandk
* Division of Developmental Neurobiology, MRC National Institute for Medical Research, The Ridgeway, Mill Hill, London NW7 1AA, UK Seto Marine Biological Laboratory, Kyoto University, Shirahama-cho, Nishimuro-gun, Wakayama 649-2211, Japan k School of Animal and Microbial Sciences, The University of Reading, Whiteknights, Reading RG6 6AJ, UK These authors contributed equally to this work Present address: Department of Developmental Neurobiology, Instituto Cajal, CSIC, Av. Doctor Arce 37, 28002 Madrid, Spain (M.M.); Stowers Institute for Medical Research, 1000 East 50th Street, Kansas City, Missouri 64110, USA (R.K.).
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The comparison of Hox genes between vertebrates and their closest invertebrate relatives (amphioxus and ascidia) highlights two derived features of Hox genes in vertebrates: duplication of the Hox gene cluster1,2, and an elaboration of Hox expression patterns and roles compared with non-vertebrate chordates38.We
have investigated how new expression domains and their associated developmental functions evolved, by testing the cis-regulatory activity of genomic DNA fragments from the cephalochordate amphioxus Hox cluster in transgenic mouse and chick embryos. Here we present evidence for the conservation of cis-regulatory mechanisms controlling gene expression in the neural tube for half a billion years of evolution, including a dependence on retinoic acid signalling. We also identify amphioxus Hox gene regulatory elements that drive spatially localized expression in vertebrate neural crest cells, in derivatives of neurogenic placodes and in branchial arches, despite the fact that cephalochordates lack both neural crest and neurogenic placodes. This implies an elaboration of cis-regulatory elements in the Hox gene cluster of vertebrate ancestors during the evolution of craniofacial patterning.
New gene-expression sites and regulatory differences may have been important in permitting the evolution of increased body-plan complexity in vertebrates. The evolution of vertebrates involved new Hox expression in neural crest and mesoderm, in addition to renement of expression domains to pattern the axial skeleton and nervous system. To investigate how vertebrate Hox gene regulation evolved, we examined the regulatory potential of genomic DNA from the amphioxus Hox cluster (AmphiHox-1 to AmphiHox-3) in vertebrate embryos. These 39 genes are homologous to Hox paralogy groups 13 of vertebrates, for which many...