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. 2009 May;26(5):1143-53.
doi: 10.1093/molbev/msp029. Epub 2009 Feb 19.

Evolution of mutation rates: phylogenomic analysis of the photolyase/cryptochrome family

José Ignacio Lucas-Lledó  1 , Michael Lynch
Affiliations

Evolution of mutation rates: phylogenomic analysis of the photolyase/cryptochrome family

José Ignacio Lucas-Lledó et al. Mol Biol Evol. 2009 May.

Abstract

Photoreactivation, one of the first DNA repair pathways to evolve, is the direct reversal of premutagenic lesions caused by ultraviolet (UV) irradiation, catalyzed by photolyases in a light-dependent, single-enzyme reaction. It has been experimentally shown that photoreactivation prevents UV mutagenesis in a broad range of species. In the absence of photoreactivation, UV-induced photolesions are repaired by the more complex and much less efficient nucleotide excision repair pathway. Despite their obvious beneficial effects, several lineages, including placental mammals, lost photolyase genes during evolution. In this study, we ask why photolyase genes have been lost in those lineages and discuss the significance of these losses in the context of the evolution of the genomic mutation rates. We first perform an extensive phylogenomic analysis of the photolyase/cryptochrome family, to assess what species lack each kind of photolyase gene. Then, we estimate the ratio of nonsynonymous to synonymous substitution rates in several groups of photolyase genes, as a proxy of the strength of purifying natural selection, and we ask whether less evolutionarily constrained photolyase genes are more likely lost. We also review functional data and compare the efficiency of different kinds of photolyases. We find that eukaryotic photolyases are, on average, less evolutionarily constrained than eubacterial ones and that the strength of natural selection is correlated with the affinity of photolyases for their substrates. We propose that the loss of photolyase genes in eukaryotic species may be due to weak natural selection and may result in a deleterious increase of their genomic mutation rates. In contrast, the loss of photolyase genes in prokaryotes may not cause an increase in the mutation rate and be neutral in most cases.

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Figures

F<sc>IG</sc>. 1.—
FIG. 1.—
Unrooted neighbor-joining tree of the photolyase/cryptochrome family. Branches are labeled first with the their bootstrap support (percentage) and, when available, with: second, the bootstrap support of an equivalent branch in the maximum parsimony consensus tree; and third, with the posterior probability of an equivalent branch, according to the Bayesian analysis. Groups with the same tone are proposed to be orthologous, based on the their complementary taxonomic distribution and their proximity, despite the lack of bootstrap support in two cases (see Discussion).
F<sc>IG</sc>. 2.—
FIG. 2.—
Comparison of the mean dN/dS estimates among photolyase paralogs (A), among kingdoms (B), and between genera with and without an observed photolyase gene loss (C). In C, only dN/dS estimates for CPD class I photolyases of eubacterial genera are used, and dN/dS values of “no-loss” genera were weighted by the evolutionary time sampled. Error bars indicate the standard error of the mean, except for Archaea in panel B, where only one dN/dS estimate was used. In that case, the error bar indicates the SD of the estimate, obtained with the bootstrap method.
F<sc>IG</sc>. 3.—
FIG. 3.—
Relationship between the binding constants of photolyases for their substrates (KA) and the dN/dS estimates obtained with the genes encoding those photolyases and their closest orthologs. Binding constant values correspond to the measures reported in table 1, or to their means and standard errors, when more than one measure is available for the same species. Measures from Escherichia coli and Salmonella typhimurium CPD class I photolyases are pooled in the same mean because the corresponding dN/dS estimate also describes both species. Horizontal error bars are SDs of dN/dS estimates, obtained by bootstrap.
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