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Unresolved orthology and peculiar coding sequence properties of lamprey genes: the KCNA gene family as test case.

Qiu H, Hildebrand F, Kuraku S, Meyer A - BMC Genomics (2011)

Bottom Line: However, molecular phylogenetic analyses, especially those including lamprey genes, have produced highly discordant results between gene families.Notably, sea lamprey KCNA sequences displayed unique codon usage pattern and amino acid composition, probably associated with exceptionally high GC-content in their coding regions.Our results suggest that secondary modifications of sequence properties unique to the lamprey lineage may be one of the factors preventing robust orthology assessments of lamprey genes, which deserves further genome-wide validation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, University of Konstanz, Konstanz, Germany.

ABSTRACT

Background: In understanding the evolutionary process of vertebrates, cyclostomes (hagfishes and lamprey) occupy crucial positions. Resolving molecular phylogenetic relationships of cyclostome genes with gnathostomes (jawed vertebrates) genes is indispensable in deciphering both the species tree and gene trees. However, molecular phylogenetic analyses, especially those including lamprey genes, have produced highly discordant results between gene families. To efficiently scrutinize this problem using partial genome assemblies of early vertebrates, we focused on the potassium voltage-gated channel, shaker-related (KCNA) family, whose members are mostly single-exon.

Results: Seven sea lamprey KCNA genes as well as six elephant shark genes were identified, and their orthologies to bony vertebrate subgroups were assessed. In contrast to robustly supported orthology of the elephant shark genes to gnathostome subgroups, clear orthology of any sea lamprey gene could not be established. Notably, sea lamprey KCNA sequences displayed unique codon usage pattern and amino acid composition, probably associated with exceptionally high GC-content in their coding regions. This lamprey-specific property of coding sequences was also observed generally for genes outside this gene family.

Conclusions: Our results suggest that secondary modifications of sequence properties unique to the lamprey lineage may be one of the factors preventing robust orthology assessments of lamprey genes, which deserves further genome-wide validation. The lamprey lineage-specific alteration of protein-coding sequence properties needs to be taken into consideration in tackling the key questions about early vertebrate evolution.

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Maximum-likelihood tree of KCNA genes rooted by invertebrate sequences. 203 amino acid sites were employed in this analysis. Statistical support values for nodes with branches leading to sea lamprey and elephant shark genes are shown with ML bootstrap values left to the slash and posterior probabilities right to the slash. "-" indicates inconsistent tree topologies between Maximum-likelihood tree and Bayesian tree.
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Figure 3: Maximum-likelihood tree of KCNA genes rooted by invertebrate sequences. 203 amino acid sites were employed in this analysis. Statistical support values for nodes with branches leading to sea lamprey and elephant shark genes are shown with ML bootstrap values left to the slash and posterior probabilities right to the slash. "-" indicates inconsistent tree topologies between Maximum-likelihood tree and Bayesian tree.

Mentions: The tree focusing on the vertebrate KCNA genes was reconstructed with the ML (Figure 3) and Bayesian inference methods (Additional file 3, Figure S3). This analysis included six sea lamprey KCNA genes and complete or nearly complete sets of KCNA sequences of three tetrapods (human, chicken and frog), one non-teleost actinopterygian fish (Florida gar), and one cartilaginous fish (elephant shark), and employed sea urchin and sea squirt homologs as an outgroup (Figure 3). The sea lamprey PmKCNAν was excluded because of its extremely divergent sequence among the deuterostome KCNA genes (Additional file 2, Figure S2). Maximum-likelihood and Bayesian inference supported tree topologies similar to that of a previous study, in terms of relationships between gnathostome KCNA subgroups [17]. In this tree, monophylies of all individual gnathostome KCNA subgroups (KCNA1-7 and 10) were strongly supported (BP: 67-99; PP: 0.91-1.00). However, instead of grouping KCNA5 and -10, which was suggested by the previously proposed evolutionary history of the KCNA clusters [17], a sister group relationship between KCNA10 and KCNA1-6 was supported by the ML tree (Figure 3). This might be due to the accelerated evolution of KCNA10 after the split between KCNA5 and -10 [17] and shorter alignment [203 amino acid sites (aa)] used in this analysis than in the previous one (364 aa) [17].


Unresolved orthology and peculiar coding sequence properties of lamprey genes: the KCNA gene family as test case.

Qiu H, Hildebrand F, Kuraku S, Meyer A - BMC Genomics (2011)

Maximum-likelihood tree of KCNA genes rooted by invertebrate sequences. 203 amino acid sites were employed in this analysis. Statistical support values for nodes with branches leading to sea lamprey and elephant shark genes are shown with ML bootstrap values left to the slash and posterior probabilities right to the slash. "-" indicates inconsistent tree topologies between Maximum-likelihood tree and Bayesian tree.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3141671&req=5

Figure 3: Maximum-likelihood tree of KCNA genes rooted by invertebrate sequences. 203 amino acid sites were employed in this analysis. Statistical support values for nodes with branches leading to sea lamprey and elephant shark genes are shown with ML bootstrap values left to the slash and posterior probabilities right to the slash. "-" indicates inconsistent tree topologies between Maximum-likelihood tree and Bayesian tree.
Mentions: The tree focusing on the vertebrate KCNA genes was reconstructed with the ML (Figure 3) and Bayesian inference methods (Additional file 3, Figure S3). This analysis included six sea lamprey KCNA genes and complete or nearly complete sets of KCNA sequences of three tetrapods (human, chicken and frog), one non-teleost actinopterygian fish (Florida gar), and one cartilaginous fish (elephant shark), and employed sea urchin and sea squirt homologs as an outgroup (Figure 3). The sea lamprey PmKCNAν was excluded because of its extremely divergent sequence among the deuterostome KCNA genes (Additional file 2, Figure S2). Maximum-likelihood and Bayesian inference supported tree topologies similar to that of a previous study, in terms of relationships between gnathostome KCNA subgroups [17]. In this tree, monophylies of all individual gnathostome KCNA subgroups (KCNA1-7 and 10) were strongly supported (BP: 67-99; PP: 0.91-1.00). However, instead of grouping KCNA5 and -10, which was suggested by the previously proposed evolutionary history of the KCNA clusters [17], a sister group relationship between KCNA10 and KCNA1-6 was supported by the ML tree (Figure 3). This might be due to the accelerated evolution of KCNA10 after the split between KCNA5 and -10 [17] and shorter alignment [203 amino acid sites (aa)] used in this analysis than in the previous one (364 aa) [17].

Bottom Line: However, molecular phylogenetic analyses, especially those including lamprey genes, have produced highly discordant results between gene families.Notably, sea lamprey KCNA sequences displayed unique codon usage pattern and amino acid composition, probably associated with exceptionally high GC-content in their coding regions.Our results suggest that secondary modifications of sequence properties unique to the lamprey lineage may be one of the factors preventing robust orthology assessments of lamprey genes, which deserves further genome-wide validation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, University of Konstanz, Konstanz, Germany.

ABSTRACT

Background: In understanding the evolutionary process of vertebrates, cyclostomes (hagfishes and lamprey) occupy crucial positions. Resolving molecular phylogenetic relationships of cyclostome genes with gnathostomes (jawed vertebrates) genes is indispensable in deciphering both the species tree and gene trees. However, molecular phylogenetic analyses, especially those including lamprey genes, have produced highly discordant results between gene families. To efficiently scrutinize this problem using partial genome assemblies of early vertebrates, we focused on the potassium voltage-gated channel, shaker-related (KCNA) family, whose members are mostly single-exon.

Results: Seven sea lamprey KCNA genes as well as six elephant shark genes were identified, and their orthologies to bony vertebrate subgroups were assessed. In contrast to robustly supported orthology of the elephant shark genes to gnathostome subgroups, clear orthology of any sea lamprey gene could not be established. Notably, sea lamprey KCNA sequences displayed unique codon usage pattern and amino acid composition, probably associated with exceptionally high GC-content in their coding regions. This lamprey-specific property of coding sequences was also observed generally for genes outside this gene family.

Conclusions: Our results suggest that secondary modifications of sequence properties unique to the lamprey lineage may be one of the factors preventing robust orthology assessments of lamprey genes, which deserves further genome-wide validation. The lamprey lineage-specific alteration of protein-coding sequence properties needs to be taken into consideration in tackling the key questions about early vertebrate evolution.

Show MeSH