Abstract

BackgroundCodon usage may vary significantly between different organisms and between genes within the same organism. Several evolutionary processes have been postulated to be the predominant determinants of codon usage: selection, mutation, and genetic drift. However, the relative contribution of each of these factors in different species remains debatable. The availability of complete genomes for tens of multicellular organisms provides an opportunity to inspect the relationship between codon usage and the evolutionary age of genes.ResultsWe assign an evolutionary age to a gene based on the relative positions of its identified homologues in a standard phylogenetic tree. This yields a classification of all genes in a genome to several evolutionary age classes. The present study starts from the observation that each age class of genes has a unique codon usage and proceeds to provide a quantitative analysis of the codon usage in these classes. This observation is made for the genomes of Homo sapiens, Mus musculus, and Drosophila melanogaster. It is even more remarkable that the differences between codon usages in different age groups exhibit similar and consistent behavior in various organisms. While we find that GC content and gene length are also associated with the evolutionary age of genes, they can provide only a partial explanation for the observed codon usage.ConclusionWhile factors such as GC content, mutational bias, and selection shape the codon usage in a genome, the evolutionary history of an organism over hundreds of millions of years is an overlooked property that is strongly linked to GC content, protein length, and, even more significantly, to the codon usage of metazoan genomes.

Highlights

  • Codon usage may vary significantly between different organisms and between genes within the same organism

  • We show a significant coupling between the evolutionary age of a gene and its codon preferences in representative metazoan genomes

  • We show that the GC content of a gene and its length are associated with its evolutionary age

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Summary

Introduction

Codon usage may vary significantly between different organisms and between genes within the same organism. Some of the main conclusions of these studies are: (i) In prokaryotes, archaea, and single-cell eukaryotes [4], translational efficiency (or fidelity) underlies the strong codon usage bias discovered for highly expressed genes [5]. This correlation is (page number not for citation purposes). BMC Evolutionary Biology 2009, 9:285 http://www.biomedcentral.com/1471-2148/9/285 valid as well in multicellular organisms, such as worms [6,7], flies, and plants [8,9], but does not hold in higher multicellular organisms [10]; (ii) There exists a strong correlation between codon usage and genomic GC content. The causal relationships between GC content, codon usage, and the underlying evolutionary constraints that may have shaped them are still not fully understood

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