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The HoxA and HoxD gene clusters of jawed vertebrates are organized into bipartite three-dimensional chromatin structures that separate long-range regulatory inputs coming from the anterior and posterior Hox-neighboring regions. This architecture is instrumental in allowing vertebrate Hox genes to pattern disparate parts of the body, including limbs. Almost nothing is known about how these three-dimensional topologies originated. Here we perform extensive 4C-seq profiling of the Hox cluster in embryos of amphioxus, an invertebrate chordate. We find that, in contrast to the architecture in vertebrates, the amphioxus Hox cluster is organized into a single chromatin interaction domain that includes long-range contacts mostly from the anterior side, bringing distant cis-regulatory elements into contact with Hox genes. We infer that the vertebrate Hox bipartite regulatory system is an evolutionary novelty generated by combining ancient long-range regulatory contacts from DNA in the anterior Hox neighborhood with new regulatory inputs from the posterior side.

Original publication

DOI

10.1038/ng.3497

Type

Journal article

Journal

Nat Genet

Publication Date

03/2016

Volume

48

Pages

336 - 341

Keywords

Animals, Body Patterning, Chromatin, Conserved Sequence, Evolution, Molecular, Extremities, Gene Expression Regulation, Developmental, Homeodomain Proteins, Lancelets, Multigene Family, Phylogeny, Vertebrates