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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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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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pone-0001567-g004: 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.

Mentions: To gain insight into the evolutionary rates of MyoD paralogues, a ML analysis was then performed, imposing the suggested correct topology of the teleost WGD (Acanthopterygian MyoD2 sequences branching internally to tetrapod MyoD orthologues but externally to teleost MyoD1 proteins: topology observed in Fig. 1d), but allowing the optimisation of branch lengths. The resulting cladogram and accompanying branch lengths can be seen in Fig. 4. Additionally, to examine differences in the evolutionary rates of MyoD paralogues and orthologues, we performed relative rate tests as described in the method section and shown in Table S1 (provided as supplementary information). X. laevis MyoD paralogues have clearly evolved asymmetrically and the branch length leading to Mf25 is around 8-fold greater than to Mf1 (Fig. 4). The relative rate test confirmed that Mf25 has evolved significantly faster than its paralogue (p = 0.002, not shown) with 24 unique substitutions relative to human MyoD compared to 7 for Mf1. Conversely, for Atlantic salmon MyoD1-co-orthologues, which are thought to have arisen from two salmonid-specific duplications of MyoD1 [5], differences in branch lengths are negligible (Fig. 4). Further, no significant differences in evolutionary rate were recorded between any two salmon MyoD1 co-orthologues in the relative rate test (Table S1). For Acanthopterygian MyoD paralogues, which almost certainly arose during the teleost WGD (see above, Fig. 2), asymmetric evolutionary rates were recorded as for X. laevis. The branch length in the Acanthopterygian MyoD2 lineage, prior to the separation of Gilthead seabream, pufferfish and sticklebacks is more than twice that of MyoD1 (Fig. 4). Additionally, evolutionary rates for individual stickleback and pufferfish MyoD2 sequences were strongly and significantly elevated compared to their MyoD1 paralogues (Fig. 4, Table S1). For example, the stickleback MyoD2 protein has 40 unique substitutions relative to human MyoD compared to 8 for MyoD1. Conversely, no significant difference in evolutionary rate was recorded between Gilthead seabream MyoD paralogues (Table S1). Interestingly, significant differences were also recorded in the evolutionary rate of MyoD2 orthologues when any two Acanthopterygian species were compared relative to human MyoD (Table S1). For example, the evolutionary rate of MyoD2 was respectively ∼4.5 and 2.5 times faster in stickleback than in Gilthead seabream and pufferfish (not shown). Conversely, differences in evolutionary rates between teleost MyoD1 orthologues were not significantly different except in one case when tiger pufferfish and zebrafish MyoD1 were compared (Table S1).


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)

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.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2215776&req=5

pone-0001567-g004: 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.
Mentions: To gain insight into the evolutionary rates of MyoD paralogues, a ML analysis was then performed, imposing the suggested correct topology of the teleost WGD (Acanthopterygian MyoD2 sequences branching internally to tetrapod MyoD orthologues but externally to teleost MyoD1 proteins: topology observed in Fig. 1d), but allowing the optimisation of branch lengths. The resulting cladogram and accompanying branch lengths can be seen in Fig. 4. Additionally, to examine differences in the evolutionary rates of MyoD paralogues and orthologues, we performed relative rate tests as described in the method section and shown in Table S1 (provided as supplementary information). X. laevis MyoD paralogues have clearly evolved asymmetrically and the branch length leading to Mf25 is around 8-fold greater than to Mf1 (Fig. 4). The relative rate test confirmed that Mf25 has evolved significantly faster than its paralogue (p = 0.002, not shown) with 24 unique substitutions relative to human MyoD compared to 7 for Mf1. Conversely, for Atlantic salmon MyoD1-co-orthologues, which are thought to have arisen from two salmonid-specific duplications of MyoD1 [5], differences in branch lengths are negligible (Fig. 4). Further, no significant differences in evolutionary rate were recorded between any two salmon MyoD1 co-orthologues in the relative rate test (Table S1). For Acanthopterygian MyoD paralogues, which almost certainly arose during the teleost WGD (see above, Fig. 2), asymmetric evolutionary rates were recorded as for X. laevis. The branch length in the Acanthopterygian MyoD2 lineage, prior to the separation of Gilthead seabream, pufferfish and sticklebacks is more than twice that of MyoD1 (Fig. 4). Additionally, evolutionary rates for individual stickleback and pufferfish MyoD2 sequences were strongly and significantly elevated compared to their MyoD1 paralogues (Fig. 4, Table S1). For example, the stickleback MyoD2 protein has 40 unique substitutions relative to human MyoD compared to 8 for MyoD1. Conversely, no significant difference in evolutionary rate was recorded between Gilthead seabream MyoD paralogues (Table S1). Interestingly, significant differences were also recorded in the evolutionary rate of MyoD2 orthologues when any two Acanthopterygian species were compared relative to human MyoD (Table S1). For example, the evolutionary rate of MyoD2 was respectively ∼4.5 and 2.5 times faster in stickleback than in Gilthead seabream and pufferfish (not shown). Conversely, differences in evolutionary rates between teleost MyoD1 orthologues were not significantly different except in one case when tiger pufferfish and zebrafish MyoD1 were compared (Table S1).

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