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WIREs Dev Biol
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Evolution of homeobox genes

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Abstract Many homeobox genes encode transcription factors with regulatory roles in animal and plant development. Homeobox genes are found in almost all eukaryotes, and have diversified into 11 gene classes and over 100 gene families in animal evolution, and 10 to 14 gene classes in plants. The largest group in animals is the ANTP class which includes the well‐known Hox genes, plus other genes implicated in development including ParaHox (Cdx, Xlox, Gsx), Evx, Dlx, En, NK4, NK3, Msx, and Nanog. Genomic data suggest that the ANTP class diversified by extensive tandem duplication to generate a large array of genes, including an NK gene cluster and a hypothetical ProtoHox gene cluster that duplicated to generate Hox and ParaHox genes. Expression and functional data suggest that NK, Hox, and ParaHox gene clusters acquired distinct roles in patterning the mesoderm, nervous system, and gut. The PRD class is also diverse and includes Pax2/5/8, Pax3/7, Pax4/6, Gsc, Hesx, Otx, Otp, and Pitx genes. PRD genes are not generally arranged in ancient genomic clusters, although the Dux, Obox, and Rhox gene clusters arose in mammalian evolution as did several non‐clustered PRD genes. Tandem duplication and genome duplication expanded the number of homeobox genes, possibly contributing to the evolution of developmental complexity, but homeobox gene loss must not be ignored. Evolutionary changes to homeobox gene expression have also been documented, including Hox gene expression patterns shifting in concert with segmental diversification in vertebrates and crustaceans, and deletion of a Pitx1 gene enhancer in pelvic‐reduced sticklebacks. WIREs Dev Biol 2013, 2:31–45. doi: 10.1002/wdev.78 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Gene Networks and Genomics Early Embryonic Development > Development to the Basic Body Plan Comparative Development and Evolution > Body Plan Evolution

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Schematic diagram demonstrating correlation between the anterior expression boundary of the Hoxc6 gene (blue domain) and the cervical–thoracic boundary in different vertebrate species. The gene is expressed at earlier developmental stages, in embryonic somites, before formation of definitive vertebrae. Occipital vertebrae, which contribute to the base of the skull, are not shown. (Based on data from Ref 95)

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Single Hox gene clusters in an insect (Drosophila melanogaster) and amphioxus (Branchiostoma floridae) are homologous to four gene clusters in human or mouse (Mus musculus). Color coding denotes division of Hox genes in ‘anterior’, ‘group 3’, ‘middle’, and ‘posterior’ groups. The group 3 gene in D. melanogaster has triplicated and diverged to give zen, zen2, and bcd. The Hox genes zen, zen2, bcd, and ftz have diverged in function and do not have homeotic roles.

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Hypothetical role of Hox, ParaHox, and NK homeobox gene clusters in patterning of neural, gut, and mesodermal tissues in an early bilaterian animal. Anterior to the left.

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Possible evolutionary history of the ANTP class homeobox genes, involving extensive tandem duplication to generate NK genes (red) and later ProtoHox genes (blue). Duplication of a hypothetical ProtoHox gene cluster (shown here as two genes, though the precise number is unresolved) gave distinct Hox and ParaHox gene clusters (blue and green, respectively).

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Evolutionary tree showing total number of homeobox genes present in the genomes of selected animal species. The precise numbers are liable to change slightly with each release of a revised genome assembly; these data from HomeoDB2 accessed December 20113 1R, 2R, and 3R denote whole genome duplication events. (Animal diagrams by Tatiana Solovieva)

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Deletion of a Pitx1 ‘pelvic enhancer’ in pelvic‐reduced sticklebacks. An enhancer region driving Pitx1 gene expression specifically in the pelvic region is located around 34 kb 5′ of the Pitx1 transcriptional start site (top line). A population of three‐spined sticklebacks from Salmon River has a complete pelvic region (shaded black) and the cis‐regulatory region is complete. Isolated freshwater populations (three examples shown) can have dramatically reduced pelvic regions, associated with deletion mutations covering or overlapping the characterized pelvic enhancer. (Based on data from Ref 102)

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Schematic diagram showing segmental specialization in three crustacean species in relation to the the expression of Ubx protein, detected using an antibody recognizing Ubx and AbdA (blue domain). The six head segments shown are Oc, ocular; A1, first antennal; A2, second antennal, Mn, mandibular; Mx1, first maxillary; Mx2, second maxillary. Only the first five trunk segments are shown (T1–T5). Segments Mn, Mx1, and Mx2 usually bear feeding appendages, and trunk segments bear locomotory appendages. In Mysidium T1, and Homarus T1 and T2, trunk segments are modified as feeding appendages, in association with absence of Ubx protein expression. Mysidium T2 has an intermediate state. (Based on data from Ref 97)

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