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Characterization of the definitive classical calpain family of vertebrates using phylogenetic, evolutionary and expression analyses.

Macqueen DJ, Wilcox AH - Open Biol (2014)

Bottom Line: We reveal that while all vertebrate classical calpains have been subject to persistent purifying selection during evolution, the degree and nature of selective pressure has often been lineage-dependent.This highlighted systematic divergence in expression across vertebrate taxa, with most classic calpain genes from fish and amphibians having more extensive tissue distribution than in amniotes.Our data suggest that classical calpain functions have frequently diverged during vertebrate evolution and challenge the ongoing value of the established system of classifying calpains by expression.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK.

ABSTRACT
The calpains are a superfamily of proteases with extensive relevance to human health and welfare. Vast research attention is given to the vertebrate 'classical' subfamily, making it surprising that the evolutionary origins, distribution and relationships of these genes is poorly characterized. Consequently, there exists uncertainty about the conservation of gene family structure, function and expression that has been principally defined from work with mammals. Here, more than 200 vertebrate classical calpains were incorporated in phylogenetic analyses spanning an unprecedented range of taxa, including jawless and cartilaginous fish. We demonstrate that the common vertebrate ancestor had at least six classical calpains, including a single gene that gave rise to CAPN11, 1, 2 and 8 in the early jawed fish lineage, plus CAPN3, 9, 12, 13 and a novel calpain gene, hereafter named CAPN17. We reveal that while all vertebrate classical calpains have been subject to persistent purifying selection during evolution, the degree and nature of selective pressure has often been lineage-dependent. The tissue expression of the complete classic calpain family was assessed in representative teleost fish, amphibians, reptiles and mammals. This highlighted systematic divergence in expression across vertebrate taxa, with most classic calpain genes from fish and amphibians having more extensive tissue distribution than in amniotes. Our data suggest that classical calpain functions have frequently diverged during vertebrate evolution and challenge the ongoing value of the established system of classifying calpains by expression.

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Bayesian phylogenetic analysis of 210 classical calpain sequences spanning vertebrate evolution. Branch lengths are relative to an uncalibrated timescale. Posterior probability values are included for every node. Boxed groups of sequences show vertebrate-wide classical calpain family members. Grey arrowheads highlight branching patterns hypothesized to be erroneous with associated text indicating the correct vertebrate-wide family member (details in main text and figure 3).
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RSOB130219F1: Bayesian phylogenetic analysis of 210 classical calpain sequences spanning vertebrate evolution. Branch lengths are relative to an uncalibrated timescale. Posterior probability values are included for every node. Boxed groups of sequences show vertebrate-wide classical calpain family members. Grey arrowheads highlight branching patterns hypothesized to be erroneous with associated text indicating the correct vertebrate-wide family member (details in main text and figure 3).

Mentions: We identified classical calpain sequences from an unprecedented range of vertebrate lineages, and more than 200 were used in a Bayesian phylogenetic analysis (figure 1). The results were consistent with several current hypotheses about classical calpain relationships [7,8,31]. However, two major branching patterns were inconsistent with previous data, or considered incorrect for other reasons (described below, see figure 1 legend). We thus also provide a consensus tree where these branching mistakes are corrected, allowing readers to rapidly absorb the phylogenetic structure of the definitive vertebrate classical calpain family according to our findings (figure 2).FigureĀ 1.


Characterization of the definitive classical calpain family of vertebrates using phylogenetic, evolutionary and expression analyses.

Macqueen DJ, Wilcox AH - Open Biol (2014)

Bayesian phylogenetic analysis of 210 classical calpain sequences spanning vertebrate evolution. Branch lengths are relative to an uncalibrated timescale. Posterior probability values are included for every node. Boxed groups of sequences show vertebrate-wide classical calpain family members. Grey arrowheads highlight branching patterns hypothesized to be erroneous with associated text indicating the correct vertebrate-wide family member (details in main text and figure 3).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4043111&req=5

RSOB130219F1: Bayesian phylogenetic analysis of 210 classical calpain sequences spanning vertebrate evolution. Branch lengths are relative to an uncalibrated timescale. Posterior probability values are included for every node. Boxed groups of sequences show vertebrate-wide classical calpain family members. Grey arrowheads highlight branching patterns hypothesized to be erroneous with associated text indicating the correct vertebrate-wide family member (details in main text and figure 3).
Mentions: We identified classical calpain sequences from an unprecedented range of vertebrate lineages, and more than 200 were used in a Bayesian phylogenetic analysis (figure 1). The results were consistent with several current hypotheses about classical calpain relationships [7,8,31]. However, two major branching patterns were inconsistent with previous data, or considered incorrect for other reasons (described below, see figure 1 legend). We thus also provide a consensus tree where these branching mistakes are corrected, allowing readers to rapidly absorb the phylogenetic structure of the definitive vertebrate classical calpain family according to our findings (figure 2).FigureĀ 1.

Bottom Line: We reveal that while all vertebrate classical calpains have been subject to persistent purifying selection during evolution, the degree and nature of selective pressure has often been lineage-dependent.This highlighted systematic divergence in expression across vertebrate taxa, with most classic calpain genes from fish and amphibians having more extensive tissue distribution than in amniotes.Our data suggest that classical calpain functions have frequently diverged during vertebrate evolution and challenge the ongoing value of the established system of classifying calpains by expression.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK.

ABSTRACT
The calpains are a superfamily of proteases with extensive relevance to human health and welfare. Vast research attention is given to the vertebrate 'classical' subfamily, making it surprising that the evolutionary origins, distribution and relationships of these genes is poorly characterized. Consequently, there exists uncertainty about the conservation of gene family structure, function and expression that has been principally defined from work with mammals. Here, more than 200 vertebrate classical calpains were incorporated in phylogenetic analyses spanning an unprecedented range of taxa, including jawless and cartilaginous fish. We demonstrate that the common vertebrate ancestor had at least six classical calpains, including a single gene that gave rise to CAPN11, 1, 2 and 8 in the early jawed fish lineage, plus CAPN3, 9, 12, 13 and a novel calpain gene, hereafter named CAPN17. We reveal that while all vertebrate classical calpains have been subject to persistent purifying selection during evolution, the degree and nature of selective pressure has often been lineage-dependent. The tissue expression of the complete classic calpain family was assessed in representative teleost fish, amphibians, reptiles and mammals. This highlighted systematic divergence in expression across vertebrate taxa, with most classic calpain genes from fish and amphibians having more extensive tissue distribution than in amniotes. Our data suggest that classical calpain functions have frequently diverged during vertebrate evolution and challenge the ongoing value of the established system of classifying calpains by expression.

Show MeSH