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PLoS One
2008 Feb 06;32:e1567. doi: 10.1371/journal.pone.0001567.
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An update on MyoD evolution in teleosts and a proposed consensus nomenclature to accommodate the tetraploidization of different vertebrate genomes.
Macqueen DJ
,
Johnston IA
.
Abstract MyoD is a muscle specific transcription factor that is essential for vertebrate myogenesis. In several teleost species, including representatives of the Salmonidae and Acanthopterygii, but not zebrafish, two or more MyoD paralogues are conserved that are thought to have arisen from distinct, possibly lineage-specific duplication events. Additionally, two MyoD paralogues have been characterised in the allotetraploid frog, Xenopus laevis. This has lead to a confusing nomenclature since MyoD paralogues have been named outside of an appropriate phylogenetic framework.Here we initially show that directly depicting the evolutionary relationships of teleost MyoD orthologues and paralogues is hindered by the asymmetric evolutionary rate of Acanthopterygian MyoD2 relative to other MyoD proteins. Thus our aim was to confidently position the event from which teleost paralogues arose in different lineages by a comparative investigation of genes neighbouring myod across the vertebrates. To this end, we show that genes on the single myod-containing chromosome of mammals and birds are retained in both zebrafish and Acanthopterygian teleosts in a striking pattern of double conserved synteny. Further, phylogenetic reconstruction of these neighbouring genes using Bayesian and maximum likelihood methods supported a common origin for teleost paralogues following the split of the Actinopterygii and Sarcopterygii.Our results strongly suggest that myod was duplicated during the basal teleost whole genome duplication event, but was subsequently lost in the Ostariophysi (zebrafish) and Protacanthopterygii lineages. We propose a sensible consensus nomenclature for vertebrate myod genes that accommodates polyploidization events in teleost and tetrapod lineages and is justified from a phylogenetic perspective.
Figure 1. Unrooted phylograms of vertebrate MyoD amino acid sequences constructed using (a) Bayesian inference with a mixed model of amino acid substitutions and assuming a gamma distribution of among-site substitution rates (b) maximum likelihood with the WAG model of amino acid substitution and assuming a gamma distribution of among-site substitution rates (gamma distribution parameter estimated by PhyML to be 0.66) with 500 psuedobootstrap replicates for branch support (c) NJ with the Poisson correction model and assuming a gamma distribution of among-site rates (gamma distribution parameter = 0.66) and 1000 bootstrap replicates for branch support (d) NJ with the Poisson correction model assuming a uniform distribution of among-site substitutions rates with 1000 bootstrap replicates for branch support.Arrows marked AS refer to the Acanthopterygian specific (AS) positioning of the teleost MyoD1/2 duplication inferred in trees a–c. The arrow marked TS shows the teleost specific (TS) positioning of the teleost MyoD1/2 duplication event in tree d. Scale bars show the number of substitutions per site. Branch confidence values >50% from the different reconstruction methods are shown.
Figure 2. Diagram depicting the synteny conserved between the myod-containing chromosome of human, with that of chicken, zebrafish, pufferfish, stickleback and medaka.A striking pattern of interleaved double conserved synteny can be seen where teleost genes are distributed between two regions as either single copies or paralogues. This, in contrast to the direct depiction of MyoD phylogenetic relationships (Fig. 1), suggests that a myod-containing chromosome duplicated in a common teleost ancestor. Genes are not scaled by size and are represented by arrows (identifying the direction of transcription) coloured by their orthology to human genes. Black arrowheads represent genes not conserved between humans and other species on the chromosomal region investigated. Double diagonal lines represent a gap of more than three genes. Teleost genes found on the two paralogous chromosomal regions are marked with a black star. The black arrow on zebrafish chromosome 7 marks the putative position where myod2 was non-functionalised. Teleost genes orthologous to those on zebrafish chromosomes 25 and 7 are respectively designated as Gene-1 and Gene-2, to identify their common paralogy. Multiple tandem tropI genes present on duplicated teleost chromosomes are labelled as a, b, c based on their left to right position and not by their inferred paralogy/orthology from phylogenetic reconstruction (Fig. 3d).
Figure 3. Unrooted phylogenetic cladograms for amino acid translations of genes in proximity to tetrapod myod that are conserved as two copies on two paralagous chromosomal regions in teleosts.Branch confidence values from different phylogenetic reconstruction methods are shown in the order they are bracketed. (a) Kcnc1 (Bayesian/ML topology). (b) Nucb2 (Bayesian/ML topology). (c) Plekha7 (Bayesian/ML topology). (d) TropI (Bayesian/ML topology). (e) Tph1 (Bayesian/ML topology). (f) Tph1 (topology corrected for mutational saturation). * represents a chromosomal duplication event arising in a common teleost ancestor. *(T1) represents the presumed first tandem duplication of tropI. Branch confidence values >50% from the different reconstruction methods are shown.
Figure 4. Unrooted ML cladogram of vertebrate MyoD amino acid sequences produced in PhyML [28] with an imposed ‘correct’ topology.The amino acid alignment was the same as used in Fig. 1. The imposed ‘correct’ starting tree topology supported the teleost WGD event (Acanthopterygii MyoD2 branching internally to tetrapod MyoD sequences, but externally to teleost MyoD1 sequences) and PhyML was used to refine branch lengths only. The ‘correct’ topology for other MyoD duplication events (in X. Laevis and Atlantic salmon) was as observed in trees in Fig. 1a–d. Branch lengths (substitutions per site) are shown above each branch.
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