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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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Alternative tree toplogies supporting different timings of two-round whole genome duplications (2R-WGDs). As an example, for a gene family with three gnathostome paralogs and three lamprey paralogs, gene trees (top) and species trees with timings of gene duplications (bottom) are shown. Gene duplications that gave rise to multiple gnathostome paralogs are indicated with grey diamond (top) and grey arrows (bottom), and those in the lamprey lineage are indicated with black diamond (top) and black arrows (bottom). Even though a recent large-scale phylogenetic analysis supported the scenario in B [4], analyses on single gene families often result in the tree topology similar to that in A. C was previously supported [49]. Abbreviations: Gna., gnathostome gene; Lam., lamprey gene; Inv., invertebrate gene.
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Figure 1: Alternative tree toplogies supporting different timings of two-round whole genome duplications (2R-WGDs). As an example, for a gene family with three gnathostome paralogs and three lamprey paralogs, gene trees (top) and species trees with timings of gene duplications (bottom) are shown. Gene duplications that gave rise to multiple gnathostome paralogs are indicated with grey diamond (top) and grey arrows (bottom), and those in the lamprey lineage are indicated with black diamond (top) and black arrows (bottom). Even though a recent large-scale phylogenetic analysis supported the scenario in B [4], analyses on single gene families often result in the tree topology similar to that in A. C was previously supported [49]. Abbreviations: Gna., gnathostome gene; Lam., lamprey gene; Inv., invertebrate gene.

Mentions: It has recently been shown that the 2R-WGDs occurred in the stem lineage leading to vertebrates after the splits of the cephalochordate and urochordate lineages [6] before the chondrichthyan lineage branched off [7]. Recently, a scenario in which both WGDs occurred before the cyclostome-gnathostome split was suggested [4]. However, there are many gene families that do not conform to the expected tree topology in phylogeny reconstructions. Often phylogenetic studies recover basal divergences and exclusive groupings of lamprey sequences with long branches (Figure 1A; see refs [8-14] for examples). This feature, observed commonly among different gene families, has also been interpreted as in support of lamprey lineage-specific genome duplication [15]. It would appear that methodological biases add to the difficulty in reconstructing the molecular phylogenies, originating from possible peculiar features of lamprey sequences, which might be preventing proper reconstructions of gene family trees.


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)

Alternative tree toplogies supporting different timings of two-round whole genome duplications (2R-WGDs). As an example, for a gene family with three gnathostome paralogs and three lamprey paralogs, gene trees (top) and species trees with timings of gene duplications (bottom) are shown. Gene duplications that gave rise to multiple gnathostome paralogs are indicated with grey diamond (top) and grey arrows (bottom), and those in the lamprey lineage are indicated with black diamond (top) and black arrows (bottom). Even though a recent large-scale phylogenetic analysis supported the scenario in B [4], analyses on single gene families often result in the tree topology similar to that in A. C was previously supported [49]. Abbreviations: Gna., gnathostome gene; Lam., lamprey gene; Inv., invertebrate gene.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Alternative tree toplogies supporting different timings of two-round whole genome duplications (2R-WGDs). As an example, for a gene family with three gnathostome paralogs and three lamprey paralogs, gene trees (top) and species trees with timings of gene duplications (bottom) are shown. Gene duplications that gave rise to multiple gnathostome paralogs are indicated with grey diamond (top) and grey arrows (bottom), and those in the lamprey lineage are indicated with black diamond (top) and black arrows (bottom). Even though a recent large-scale phylogenetic analysis supported the scenario in B [4], analyses on single gene families often result in the tree topology similar to that in A. C was previously supported [49]. Abbreviations: Gna., gnathostome gene; Lam., lamprey gene; Inv., invertebrate gene.
Mentions: It has recently been shown that the 2R-WGDs occurred in the stem lineage leading to vertebrates after the splits of the cephalochordate and urochordate lineages [6] before the chondrichthyan lineage branched off [7]. Recently, a scenario in which both WGDs occurred before the cyclostome-gnathostome split was suggested [4]. However, there are many gene families that do not conform to the expected tree topology in phylogeny reconstructions. Often phylogenetic studies recover basal divergences and exclusive groupings of lamprey sequences with long branches (Figure 1A; see refs [8-14] for examples). This feature, observed commonly among different gene families, has also been interpreted as in support of lamprey lineage-specific genome duplication [15]. It would appear that methodological biases add to the difficulty in reconstructing the molecular phylogenies, originating from possible peculiar features of lamprey sequences, which might be preventing proper reconstructions of gene family trees.

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