Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
PLoS One
2008 Feb 06;32:e1567. doi: 10.1371/journal.pone.0001567.
Show Gene links
Show Anatomy links
An update on MyoD evolution in teleosts and a proposed consensus nomenclature to accommodate the tetraploidization of different vertebrate genomes.
Macqueen DJ
,
Johnston IA
.
???displayArticle.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.
???displayArticle.pubmedLink???
18253507
???displayArticle.pmcLink???PMC2215776 ???displayArticle.link???PLoS One
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.
Atchley,
Molecular evolution of the MyoD family of transcription factors.
1994, Pubmed
Atchley,
Molecular evolution of the MyoD family of transcription factors.
1994,
Pubmed
Fares,
Rate asymmetry after genome duplication causes substantial long-branch attraction artifacts in the phylogeny of Saccharomyces species.
2006,
Pubmed
Fernandes,
Differential regulation of multiple alternatively spliced transcripts of MyoD.
2007,
Pubmed
,
Xenbase
Guindon,
A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.
2003,
Pubmed
Hall,
Temperature and the expression of seven muscle-specific protein genes during embryogenesis in the Atlantic cod Gadus morhua L.
2003,
Pubmed
Jaillon,
Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype.
2004,
Pubmed
Kassar-Duchossoy,
Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice.
2004,
Pubmed
Lin,
Muscle-specific expression of the troponin I gene requires interactions between helix-loop-helix muscle regulatory factors and ubiquitous transcription factors.
1991,
Pubmed
Macqueen,
Temperature influences the coordinated expression of myogenic regulatory factors during embryonic myogenesis in Atlantic salmon (Salmo salar L.).
2007,
Pubmed
Macqueen,
A novel salmonid myoD gene is distinctly regulated during development and probably arose by duplication after the genome tetraploidization.
2006,
Pubmed
Meyer,
Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions.
1999,
Pubmed
Notredame,
T-Coffee: A novel method for fast and accurate multiple sequence alignment.
2000,
Pubmed
Otto,
Polyploid incidence and evolution.
2000,
Pubmed
Pownall,
Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos.
2002,
Pubmed
Rescan,
Genome of the rainbow trout (Oncorhynchus mykiss) encodes two distinct muscle regulatory factors with homology to myoD.
1996,
Pubmed
Ronquist,
MrBayes 3: Bayesian phylogenetic inference under mixed models.
2003,
Pubmed
Scales,
Two distinct Xenopus genes with homology to MyoD1 are expressed before somite formation in early embryogenesis.
1990,
Pubmed
,
Xenbase
Spring,
Vertebrate evolution by interspecific hybridisation--are we polyploid?
1997,
Pubmed
Steinke,
Many genes in fish have species-specific asymmetric rates of molecular evolution.
2006,
Pubmed
Tajima,
Simple methods for testing the molecular evolutionary clock hypothesis.
1993,
Pubmed
Tamura,
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.
2007,
Pubmed
Tan,
Differential expression of two MyoD genes in fast and slow muscles of gilthead seabream ( Sparus aurata).
2002,
Pubmed
Tapscott,
The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription.
2005,
Pubmed
Taylor,
Genome duplication, a trait shared by 22000 species of ray-finned fish.
2003,
Pubmed
,
Xenbase
Van de Peer,
Dealing with saturation at the amino acid level: a case study based on anciently duplicated zebrafish genes.
2002,
Pubmed
Van de Peer,
Tetraodon genome confirms Takifugu findings: most fish are ancient polyploids.
2004,
Pubmed
Weinberg,
Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos.
1996,
Pubmed
Woods,
The zebrafish gene map defines ancestral vertebrate chromosomes.
2005,
Pubmed
