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      Genesis and evolution of the Evx and Mox genes and the extended Hox and ParaHox gene clusters

      research-article
      1 , 2 , 1 ,
      Genome Biology
      BioMed Central

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          Abstract

          The origin and evolution of genes belonging to the extended Hox group of homeobox-containing genes, namely Mox and Evx, is obscure. Here, a scenario is proposed in which an Evx/Mox ancestor gene linked to a ProtoHox cluster was involved in a segmental tandem duplication event that generated an array of all Hox-like genes.

          Abstract

          Background

          Hox and ParaHox gene clusters are thought to have resulted from the duplication of a ProtoHox gene cluster early in metazoan evolution. However, the origin and evolution of the other genes belonging to the extended Hox group of homeobox-containing genes, that is, Mox and Evx, remains obscure. We constructed phylogenetic trees with mouse, amphioxus and Drosophila extended Hox and other related Antennapedia-type homeobox gene sequences and analyzed the linkage data available for such genes.

          Results

          We claim that neither Mox nor Evx is a Hox or ParaHox gene. We propose a scenario that reconciles phylogeny with linkage data, in which an Evx/Mox ancestor gene linked to a ProtoHox cluster was involved in a segmental tandem duplication event that generated an array of all Hox-like genes, referred to as the 'coupled' cluster. A chromosomal breakage within this cluster explains the current composition of the extended Hox cluster (with Evx, Hox and Mox genes) and the ParaHox cluster.

          Conclusions

          Most studies dealing with the origin and evolution of Hox and ParaHox clusters have not included the Hox-related genes Mox and Evx. Our phylogenetic analyses and the available linkage data in mammalian genomes support an evolutionary scenario in which an ancestor of Evx and Mox was linked to the ProtoHox cluster, and that a tandem duplication of a large genomic region early in metazoan evolution generated the Hox and ParaHox clusters, plus the cluster-neighbors Evx and Mox. The large 'coupled' Hox-like cluster EvxHox/ MoxParaHox was subsequently broken, thus grouping the Mox and Evx genes to the Hox clusters, and isolating the ParaHox cluster.

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          Most cited references15

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          MEGA2: molecular evolutionary genetics analysis software.

          We have developed a new software package, Molecular Evolutionary Genetics Analysis version 2 (MEGA2), for exploring and analyzing aligned DNA or protein sequences from an evolutionary perspective. MEGA2 vastly extends the capabilities of MEGA version 1 by: (1) facilitating analyses of large datasets; (2) enabling creation and analyses of groups of sequences; (3) enabling specification of domains and genes; (4) expanding the repertoire of statistical methods for molecular evolutionary studies; and (5) adding new modules for visual representation of input data and output results on the Microsoft Windows platform. http://www.megasoftware.net. s.kumar@asu.edu
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            Zebrafish hox clusters and vertebrate genome evolution.

            HOX genes specify cell fate in the anterior-posterior axis of animal embryos. Invertebrate chordates have one HOX cluster, but mammals have four, suggesting that cluster duplication facilitated the evolution of vertebrate body plans. This report shows that zebrafish have seven hox clusters. Phylogenetic analysis and genetic mapping suggest a chromosome doubling event, probably by whole genome duplication, after the divergence of ray-finned and lobe-finned fishes but before the teleost radiation. Thus, teleosts, the most species-rich group of vertebrates, appear to have more copies of these developmental regulatory genes than do mammals, despite less complexity in the anterior-posterior axis.
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              Archetypal organization of the amphioxus Hox gene cluster.

              Organization into gene clusters is an essential and diagnostic feature of Hox genes. Insect and nematode genomes possess single Hox gene clusters (split in Drosophila); in mammals, there are 38 Hox genes in four clusters on different chromosomes. A collinear relationship between chromosomal position, activation time and anterior expression limit of vertebrate Hox genes suggests that clustering may be important for precise spatiotemporal gene regulation and hence embryonic patterning. Hox genes have a wide phylogenetic distribution within the metazoa, and are implicated in the control of regionalization along the anteroposterior body axis. It has been suggested that changes in Hox gene number and genomic organization played a role in metazoan body-plan evolution, but identifying significant changes is difficult because Hox gene organization is known from only very few and widely divergent taxa (principally insects, nematodes and vertebrates). Here we analyse the complexity and organization of Hox genes in a cephalochordate, amphioxus, the taxon thought to be the sister group of the vertebrates. We find that the amphioxus genome has only one Hox gene cluster. It has similar genomic organization to the four mammalian Hox clusters, and contains homologues of at least the first ten paralogous groups of vertebrate Hox genes in a collinear array. Remarkably, this organization is compatible with that inferred for a direct ancestor of the vertebrates; we conclude that amphioxus is a living representative of a critical intermediate stage in Hox cluster evolution.
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                Author and article information

                Journal
                Genome Biol
                Genome Biology
                BioMed Central
                1465-6906
                1465-6914
                2003
                23 January 2003
                : 4
                : 2
                : R12
                Affiliations
                [1 ]Departament de Genètica, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 645, E-08028 Barcelona, Spain
                [2 ]Current address: Division of Developmental Biology, National Institute for Medical Research, The Ridgeway, Mill Hill, London NW7 1AA, UK
                Correspondence: Jordi Garcia-Fernàndez. E-mail: jgarcia@bio.ub.es
                Article
                gb-2003-4-2-r12
                10.1186/gb-2003-4-2-r12
                151302
                12620122
                6fa93413-6a22-43e5-945e-541f960c7126
                Copyright © 2003 Minguillón and Garcia-Fernàndez; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL
                History
                : 24 September 2002
                : 31 October 2002
                : 9 December 2002
                Categories
                Research

                Genetics
                Genetics

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