Abstract

BackgroundGenes are created by a variety of evolutionary processes, some of which generate duplicate copies of an entire gene, while others rearrange pre-existing genetic elements or co-opt previously non-coding sequence to create genes with 'novel' sequences. These novel genes are thought to contribute to distinct phenotypes that distinguish organisms. The creation, evolution, and function of duplicated genes are well-studied; however, the genesis and early evolution of novel genes are not well-characterized. We developed a computational approach to investigate these issues by integrating genome-wide comparative phylogenetic analysis with functional and interaction data derived from small-scale and high-throughput experiments.ResultsWe examine the function and evolution of new genes in the yeast Saccharomyces cerevisiae. We observed significant differences in the functional attributes and interactions of genes created at different times and by different mechanisms. Novel genes are initially less integrated into cellular networks than duplicate genes, but they appear to gain functions and interactions more quickly than duplicates. Recently created duplicated genes show evidence of adapting existing functions to environmental changes, while young novel genes do not exhibit enrichment for any particular functions. Finally, we found a significant preference for genes to interact with other genes of similar age and origin.ConclusionsOur results suggest a strong relationship between how and when genes are created and the roles they play in the cell. Overall, genes tend to become more integrated into the functional networks of the cell with time, but the dynamics of this process differ significantly between duplicate and novel genes.

Highlights

  • Genes are created by a variety of evolutionary processes, some of which generate duplicate copies of an entire gene, while others rearrange pre-existing genetic elements or co-opt previously non-coding sequence to create genes with ‘novel’ sequences

  • We classified all genes in S. cerevisiae into one of three ‘age’ categories: pre-whole-genome duplication (WGD) genes that were present before the WGD event approximately 100150 million years ago; WGD genes that were duplicated by the WGD and maintained; and post-WGD genes that have appeared since the WGD

  • Genes present before the WGD will be referred to as ‘old’, while those created since the WGD will, in comparison, be referred to as ‘young’ or ‘recently created’

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Summary

Introduction

Genes are created by a variety of evolutionary processes, some of which generate duplicate copies of an entire gene, while others rearrange pre-existing genetic elements or co-opt previously non-coding sequence to create genes with ‘novel’ sequences. These novel genes are thought to contribute to distinct phenotypes that distinguish organisms. Whereas duplicate genes typically retain significant homology to their parent genes, evolutionary mechanisms like domain shuffling and gene fission and fusion can generate genes with new combinations of pre-existing functional elements [8,10]. De novo gene creation from non-coding sequence is increasingly recognized as an important source of new genes. As more genomes have been sequenced, the prevalence of ‘orphan’ genes, with little to no similarity to other known genes, has not decreased; they still represent around 10-20% of all known genes [18,19,20,21]

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