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.2011 Jun 16:11:169.
doi: 10.1186/1471-2148-11-169.

The dynamics of vertebrate homeobox gene evolution: gain and loss of genes in mouse and human lineages

Affiliations

The dynamics of vertebrate homeobox gene evolution: gain and loss of genes in mouse and human lineages

Ying-fu Zhong et al. BMC Evol Biol..

Erratum in

  • BMC Evol Biol. 2011;11:204

Abstract

Background: Homeobox genes are a large and diverse group of genes, many of which play important roles in transcriptional regulation during embryonic development. Comparison of homeobox genes between species may provide insights into the evolution of developmental mechanisms.

Results: Here we report an extensive survey of human and mouse homeobox genes based on their most recent genome assemblies, providing the first comprehensive analysis of mouse homeobox genes and updating an earlier survey of human homeobox genes. In total we recognize 333 human homeobox loci comprising 255 probable genes and 78 probable pseudogenes, and 324 mouse homeobox loci comprising 279 probable genes and 45 probable pseudogenes (accessible at http://homeodb.zoo.ox.ac.uk). Comparison to partial genome sequences from other species allows us to resolve which differences are due to gain of genes and which are due to gene losses.

Conclusions: We find there has been much more homeobox gene loss in the rodent evolutionary lineage than in the primate lineage. While humans have lost only the Msx3 gene, mice have lost Ventx, Argfx, Dprx, Shox, Rax2, LOC647589, Tprx1 and Nanognb. This analysis provides insight into the patterns of homeobox gene evolution in the mammals, and a step towards relating genomic evolution to phenotypic evolution.

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Figures

Figure 1
Figure 1
Chromosomal distribution of humanDUX4-like genes and mouse 'chromosome 10' Dux Genes. (A) Twenty-three humanDUX4-like sequences include four loci with predicted introns interrupting the coding sequence (orange arrows) and nineteen intronless sequences (grey arrows), most clustering on chromosomes 4, 10 and Y. One putative intron-containing locus at chromosome 10q26.3 is disrupted by a translocation or is the remnants of two loci. (B) The Dux gene on mouse chromosome 10 has been duplicated in tandem to generate three loci. Orientation of arrows indicates direction of transcription; small arrowheads indicate putative introns.
Figure 2
Figure 2
DUXBandCPHXloci in mouse and human. (A) MouseDUXB-like(Duxbl, orange arrows) andCphx(red arrows), together with a non-homeobox genePlac9(green arrows), have been duplicated giving three copies each at chromosome 14A3. (B) HumanCphx-related homeobox loci flank aDUXBLpseudogene and theDUXBgene on chromosomes 10 and 16 respectively, although the loci on chromosome 10 are disrupted (ragged boxes).Anxa11(blue arrows) is not a homeobox genes. (C) Amino acid alignments; dots represent identical amino acids, dashes deletons/insertions and red characters conservative substitutions. Hs,Homo sapiens; Mm,Mus musculus.
Figure 3
Figure 3
Presence or absence of theNANOGNBgene in mammalian genomes. (A) The deduced homeodomain sequence of humanNANOGNBshowing predicted alpha helical regions, compatible with folding into a homeodomain tertiary structure. (B)NANOGNBis located just 15 kb from the humanNANOGgene at chromosome 12p13.31 (orange arrows). Orthologous genes at the syntenic position are present in horse and dog, but not in mouse and rat. Grey arrows indicate non-homeobox genes.
Figure 4
Figure 4
Absence ofLOC647589in the mouse genome.LOC647589was detected in this study at human chromosome 12q24.33. No annotation is found in genomes outside of human currently, although a homologous sequences is present in cow (chr17:46,768,917-46,783,902) and other mammals with available genome sequences, but not in mouse or rat. The orange arrow and box indicate homeobox loci; grey arrows indicate non-homeobox genes.
Figure 5
Figure 5
Rhox (reproductive homeobox) gene clusters. (A) Three Rhox loci are present in the human genome at chromosome Xq24. (B) Thirty-six Rhox loci are clustered in the mouse genome at chromosome X A3.3.Rhox3-ps(white arrow) has a stop codon in the homeobox.
Figure 6
Figure 6
Origin of theLEUTXgene in the human genome. TheLEUTXhomeobox gene (orange arrow) plus four unusual non-homeobox genes (light grey arrows) form a linked set of genes in the human genome (dashed box). These genes are not present at the syntenic location in mouse, rat, cow or dog genomes.
Figure 7
Figure 7
The mouse Obox loci and associated genes. There are 36 mouse Obox homeobox loci, comprising 6 intron-containing genes (orange arrows) and 28 intronless loci (unfilled arrows) on chromosome 7, plus intronless probable pseudogenes on chromosome 17. Four other homeobox genes, not clearly part of the Obox family, are linked to the large Obox cluster:Crxos1, Gm5585andGm7235andCrx(red arrows).
Figure 8
Figure 8
TheMSX3gene has been lost in human and dog genomes. TheMsx3gene is located in syntenic regions of mouse, rat and pig genomes (orange arrows), but absent at the equivalent location in human and pig. Non-homeobox genes used as indicators of chromosomal synteny are shown as grey arrows.
Figure 9
Figure 9
TheVentxgene has been lost in rodent genomes. TheVENTXgene is located in syntenic regions of human, rat, dog and chicken genomes (orange arrows), but absent at the equivalent location in mouse and rat. Non-homeobox genes used as indicators of chromosomal synteny are shown as grey arrows.
Figure 10
Figure 10
TheARGFXlocus has been lost in rodent genomes. TheARGFXgene is located in syntenic regions of human and cow (orange arrows), but absent at the equivalent location in mouse and rat. Non-homeobox genes used as indicators of chromosomal synteny are shown as grey arrows.
Figure 11
Figure 11
TheDPRXgene has been lost in rodent genomes. TheDPRXgene is located in syntenic regions of human, dog and horse (orange arrows), but absent at the equivalent location in mouse and rat. Non-homeobox genes used as indicators of chromosomal synteny are shown as grey arrows.
Figure 12
Figure 12
TheSHOXgene has been lost in rodent genomes. TheSHOXgene is located in syntenic regions of human (X and Y chromosomes) and chicken (orange arrows), but absent at the equivalent location in mouse and rat. Non-homeobox genes used as indicators of chromosomal synteny are shown as grey arrows.
Figure 13
Figure 13
TheRAX2gene has been lost in rodent genomes. TheRAX2gene is located in syntenic regions of human and chicken (orange arrows), but absent at the equivalent location in mouse and rat. Non-homeobox genes used as indicators of chromosomal synteny are shown as grey arrows.
Figure 14
Figure 14
Tprx loci are not present in rodent genomes. In the human genome, the Tprx family contains one probable functional gene (TPRX1) and a possibly non-functional tandem duplicate (TPRX2P) at chromosome 19q13, either side of the Otx-familyCRXgene. The additional Tprx loci,TPRX1P1, TPRX1P2andTPRXL,are elsewhere in the genome and are not shown. Examination of the region syntenic to human 19q13 in other mammals reveals clear orthologues of Tprx family loci in cow and dog, but not mouse and rat. In rodents, another homeobox geneCrxos1is found. Orange arrows indicate homeobox genes; grey arrows are non-homeobox genes.
Figure 15
Figure 15
A summary of homeobox gene dynamics in the mouse and human evolutionary lineages. The majority of homeobox genes are conserved between mouse and human lineages (grey squares), although some have undergone duplication to different extents (cascaded boxes). Humans have lost theMsx3gene; mice have lostVENTX, ARGFX, DPRX, SHOX, RAX2, LOC647589, NANOGBandTPRX1(dashed boxes). Three new homeobox loci (Gm7235, Gm5585andCrxos1) and one new cluster (Obox) arose in the rodent lineage; one new geneLeutxarose in the lineage leading to primates.
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