Academic journal article Genetics

Copy Correction and Concerted Evolution in the Conservation of Yeast Genes

Academic journal article Genetics

Copy Correction and Concerted Evolution in the Conservation of Yeast Genes

Article excerpt

ABSTRACT

The yeast Saccharomyces cerevisiae and other members of the genus Saccharomyces are descendants of an ancient whole-genome duplication event. Although most of the duplicate genes have since been deleted, many remain, and so there are many pairs of related genes. We have found that poorly expressed genes diverge rapidly from their paralog, while highly expressed genes diverge little, if at all. This lack of divergence of highly expressed paralogous gene pairs seems to involve gene correction: one member of the pair "corrects" the sequence of its twin, and so the gene pair evolves as a unit. This correction presumably involves gene conversion and could occur via a reverse-transcribed cDNA intermediate. Such correction events may also occur in other organisms. These results support the idea that copies of poorly expressed genes are preserved when they diverge to take on new functions, while copies of highly expressed genes are preserved when they are needed to provide additional gene product for the original function.

IT is generally believed that selection for preferred codons (codon bias) increases the sequence conservation of highly expressed genes relative to poorly expressed genes (the "selection hypothesis") (POWELL and MORIYAMA 1997). Both highly expressed and poorly expressed genes are selected for function, which means that many nonsynonymous codon changes are selected against; but in addition, for highly expressed genes, many synonymous changes are also selected against to maintain codons preferred for translational efficiency and accuracy. A corollary of this argument is that when an organism has two similar copies of a highly expressed gene, these copies should be preserved in evolution as a gene pair sharing high homology, because selection for both function and codon bias prevents the members of the pair from drifting apart.

In this study, we propose a parallel hypothesis for the conservation of duplicated highly expressed genes and show that the new hypothesis not only plays a significant role, at least in yeast, but also may be more important than selection under certain conditions.

We call our hypothesis the correction hypothesis. It consists of three proposals: first, that one copy of a gene can correct the sequence of a second copy; second, that correction depends on high sequence identity; and third, that the probability of correction depends on the level of gene expression. We propose two possible mechanisms of correction. In the first, correction happens through the occasional copying back of mature mRNA into cDNA using reverse transcriptase and a subsequent recombinational interaction between the cDNA and the second copy of the chromosomal gene. In the second mechanism, correction is due to a direct recombinational interaction between the two genes of a duplicate pair.

In the following sections, we first show that correction indeed plays a significant role in the conservation of gene pairs in yeast and that correction is correlated with the level of gene expression. Evidence for correction is, first, that the conservation between the members of a highly expressed gene pair is too high to be explained by selection alone, and second, that the pattern of nucleotide substitution within and between species of Saccharomyces is much more compatible with the correction hypothesis than with the selection hypothesis. We examine some properties of correction and consider whether correction might play a role in other organisms.

MATERIALS AND METHODS

Saccharomyces sequences were obtained from the Saccharomyces Genome Database (http://www.yeastgenome.org/), from Washington University (http://www.genome.wustl.edu/ projects/yeast/ and http^www.genome.wustl.edu/blast/yeasL client.cgi), and from the Massachusetts Institute of Technology (http://www-genome.wi.mit.edu/seq/Saccharomyces/). ClustalW-based end-to-end fungal alignments of the Saccharomyces cerevisiae genes and their analogous sequences in the other Saccharomyces species were obtained from the Saccharomyces Genome Database (SGD; http://www. …

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