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Molecular Evolution of Teleost Neural Isozymes

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Abstract

Isozymes, homologous enzymes coded by separate loci within a genome, present interesting systems for examining molecular and functional divergence through natural selection. Isozyme pairs for a number of metabolic enzymes, including Triosephosphate isomerase (Tpi), Malate dehydrogenase (Mdh), Phosphoglucose isomerase (Pgi), and Guanylate kinase (Guk), appear to all result from a single, large duplication event early in teleost evolution. These small gene families include two forms, a generally expressed form with no apparent charge and a neurally expressed form with a pronounced negative charge although the canalization of expression of the second form varies across families. Using ancestral sequence reconstructions and standard comparisons of rates of nonsynonymous and synonymous change, combined with the examination of the specific amino acid changes observed and predicted we examined the evolution of the Tpi and Guk families using all available vertebrate sequences and all four families using a smaller, common, dataset. We find that post-duplication, the neural Tpi and Guk isozymes evolved through similar periods of positive selection as evidenced by elevated rates of nonsynonymous change and accumulation of negative amino acids. Over the same evolutionary period our analysis suggests that Mdh and Pgi isozymes appear to have evolved under a less divergent pattern of selection. These distinct results likely reflect functional differences between the isozymes, possibly a result of differences in expression patterns.

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Acknowledgments

We thank Teresa Rzezniczak, David Bing, Jose Knee, Brendan McConkey, Katharine Coykendall, and Efe Sezgin for constructive comments on this manuscript, as well as Jennifer Fenske and Stefan Siemann for phylogenetic and protein structure assistance. This study was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery (3414-07) and a Canada Research Chair (950-215763) to TJSM.

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The authors declare that they have no conflict of interest.

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  1. Department of Chemistry and Biochemistry, Laurentian University, Sudbury, ON, P3E 2C6, Canada

    Ryan R. Auld & Thomas J. S. Merritt

  2. Department of Biological Sciences, University of South Carolina, Columbia, SC, USA

    Joseph M. Quattro

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  1. Ryan R. Auld
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Correspondence to Thomas J. S. Merritt.

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Online Resource Fig. 1

Phylogenetic tree produced from the large Tpi nucleotide sequence dataset by NJ, Bayesian, and ML methods. Above each branch, proportions of 1,000 bootstrap replicates for NJ, Bayesian, and ML methods are shown. Asterisk represent nodes without bootstrap support due to separate topology being inferred by given phylogenetic method (see “Results” section)

Online Resource Fig. 2

Phylogenetic tree produced from the large Guk nucleotide sequence dataset by NJ, Bayesian, and ML methods. Above each branch, proportions of 1,000 bootstrap replicates for NJ, Bayesian, and ML methods are shown. Asterisk represent nodes without bootstrap support due to separate topology being inferred by the given phylogenetic method. The given topology is consistent with what is known from the related gene families in the teleost family, such as Tpi, Mdh, and Pgi

Online Resource Fig. 3

Phylogenetic trees of comparison datasets by NJ, Bayesian, and ML methods with 1,000 bootstrap replicate support respectively along each branch for Tpi (a), Guk (b), Mdh (c), and Pgi (d). Both Guk and Tpi comparison dataset produce identical topologies by all three phylogenetic methods, while Mdh and Pgi produced the shown topologies for two of the three phylogenetic methods. Asterisk represents nodes that were unresolved by the given phylogenetic methods

Online Resource Fig. 4

(Tpi) Inferred amino acid sequences for the duplication node (AncestralS), node leading to the neural (AncestralN), and general (AncestralG) isozyme branches of the common Tpi tree. Highlighted amino acids were found to reside on the outside of the protein by solvent accessibility of >25 %. Asterisks indicate amino acid substitutions toward negative amino acids, and isoelectric points are shown as the 3′ end of the proteins

Online Resource Fig. 5

(Mdh) Inferred amino acid sequences for the duplication node (AncestralS), node leading to the neural (AncestralN), and general (AncestralG) isozyme branches of the common Mdh tree. Highlighted amino acids were found to reside on the outside of the protein by solvent accessibility of >25 %. Asterisks indicate amino acid substitutions toward negative amino acids, and isoelectric points are shown as the 3′ end of the proteins

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Auld, R.R., Quattro, J.M. & Merritt, T.J.S. Molecular Evolution of Teleost Neural Isozymes. J Mol Evol 75, 198–213 (2012). https://doi.org/10.1007/s00239-012-9532-1

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