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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 - PLoS ONE (2008)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Gatty Marine Laboratory, School of Biology, University of St Andrews, St Andrews, Fife, Scotland.

ABSTRACT

Background: 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.

Methods and principal findings: 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.

Conclusion: 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.

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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).
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pone-0001567-g002: 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).

Mentions: Our next aim involved establishing the chromosomal locations of genes in proximity to myod in human, relative to their positions in chicken, zebrafish and three Acanthopterygian species. This information was used construct a diagram of conserved synteny across the vertebrates (Fig. 2). Additionally, since tropT and tropI genes are in direct 3′ proximity to all teleost myod genes, we also assessed their location in human and chicken genomes. A very high degree of synteny is retained between the myod containing regions of human chromosome 11 and chicken chromosome 5 (Fig. 2). Comparing these regions with teleosts, while some inter and intra chromosomal rearrangements have occurred, a striking pattern of double conserved synteny (DCS) is observed where teleost genes are found as either single copies interspersed between two paralogous chromosomal tracts (otog, abcc-8, kcnj11, pik3c2a, rps13, sergef) or as at least two paralogues on both chromosomes (tropT, tropI, tph1, kcnc1 [zebrafish specific], nucb2, plekha7) (Fig. 2). This pattern was maintained for genes found in both upstream and downstream proximity to myod in human/chicken and importantly, was observed in zebrafish (Ostariophysi) and the three Acanthopterygian species studied (Fig. 2). This common pattern of interleaved-DCS in teleosts is most consistent with the duplication of a myod-containing chromosome in a common ancestor to zebrafish (Ostariophysi) and the Acanthopterygii, but not tetrapods. We suggest that this occurred during the WGD of basal teleost evolution [9]. However, on zebrafish chromosome 5, the duplicated myod2 gene is absent relative to its inferred position from Acanthopterygian genomes (Fig. 2, black arrow). The differential retention/loss of paralogues in different teleost lineages following the WGD is surprisingly common. For example, it was shown that ∼50% of zebrafish duplicates were retained as single copies in pufferfish genomes [18], [19]. Thus to summarise, the synteny conserved between myod neighbouring genes of tetrapods relative to teleosts strongly favours a teleost specific duplication of a myod containing chromosome in direct contradiction to the majority of topologies retrieved by direct phylogenetic reconstruction (e.g. Fig. 1).


An update on MyoD evolution in teleosts and a proposed consensus nomenclature to accommodate the tetraploidization of different vertebrate genomes.

Macqueen DJ, Johnston IA - PLoS ONE (2008)

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).
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getmorefigures.php?uid=PMC2215776&req=5

pone-0001567-g002: 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).
Mentions: Our next aim involved establishing the chromosomal locations of genes in proximity to myod in human, relative to their positions in chicken, zebrafish and three Acanthopterygian species. This information was used construct a diagram of conserved synteny across the vertebrates (Fig. 2). Additionally, since tropT and tropI genes are in direct 3′ proximity to all teleost myod genes, we also assessed their location in human and chicken genomes. A very high degree of synteny is retained between the myod containing regions of human chromosome 11 and chicken chromosome 5 (Fig. 2). Comparing these regions with teleosts, while some inter and intra chromosomal rearrangements have occurred, a striking pattern of double conserved synteny (DCS) is observed where teleost genes are found as either single copies interspersed between two paralogous chromosomal tracts (otog, abcc-8, kcnj11, pik3c2a, rps13, sergef) or as at least two paralogues on both chromosomes (tropT, tropI, tph1, kcnc1 [zebrafish specific], nucb2, plekha7) (Fig. 2). This pattern was maintained for genes found in both upstream and downstream proximity to myod in human/chicken and importantly, was observed in zebrafish (Ostariophysi) and the three Acanthopterygian species studied (Fig. 2). This common pattern of interleaved-DCS in teleosts is most consistent with the duplication of a myod-containing chromosome in a common ancestor to zebrafish (Ostariophysi) and the Acanthopterygii, but not tetrapods. We suggest that this occurred during the WGD of basal teleost evolution [9]. However, on zebrafish chromosome 5, the duplicated myod2 gene is absent relative to its inferred position from Acanthopterygian genomes (Fig. 2, black arrow). The differential retention/loss of paralogues in different teleost lineages following the WGD is surprisingly common. For example, it was shown that ∼50% of zebrafish duplicates were retained as single copies in pufferfish genomes [18], [19]. Thus to summarise, the synteny conserved between myod neighbouring genes of tetrapods relative to teleosts strongly favours a teleost specific duplication of a myod containing chromosome in direct contradiction to the majority of topologies retrieved by direct phylogenetic reconstruction (e.g. Fig. 1).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Gatty Marine Laboratory, School of Biology, University of St Andrews, St Andrews, Fife, Scotland.

ABSTRACT

Background: 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.

Methods and principal findings: 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.

Conclusion: 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.

Show MeSH