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MBE Advance Access published online on September 8, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msj015
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© The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oupjournals.org
Accepted September 1, 2005

Research Article

Higher Duplicability of Less Important Genes in Yeast Genomes

Xionglei He 1 and Jianzhi Zhang 1*

1 Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA

* To whom correspondence should be addressed.
Jianzhi Zhang, E-mail: jianzhi{at}umich.edu


  Abstract

Gene duplication plays an important role in evolution because it is the primary source of new genes. Many recent studies showed that gene duplicability varies considerably among genes. Several considerations led us to hypothesize that less important genes have higher rates of successful duplications, where gene importance is measured by the fitness reduction caused by the deletion of the gene. Here we test this hypothesis by comparing the importance of two groups of singleton genes in the yeast Saccharomyces cerevisiae. Group S genes did not duplicate in four other yeast species examined, whereas group D experienced duplication in these species. Consistent with our hypothesis, we found group D genes to be less important than group S genes. Specifically, 17% of group D genes are essential in S. cerevisiae, compared to 28% for group S. Furthermore, deleting a group D gene in S. cerevisiae reduces the fitness by 24% on average, compared to 38% for group S. Our subsequent analysis showed that less important genes have more cis-regulatory motifs, which could lead to a higher chance of subfunctionalization of duplicate genes and result in an enhanced rate of gene retention. Less important genes may also have weaker dosage imbalance effects and cause fewer genetic perturbations when duplicated. Regardless of the cause, our observation indicates that the previous finding of a less severe fitness consequence of deleting a duplicate gene than deleting a singleton gene is at least in part due to the fact that duplicate genes are intrinsically less important than singleton genes and suggests that the contribution of duplicate genes to genetic robustness has been overestimated.

Keywords: gene duplicability; yeast; gene dispensability; gene importance; functional compensation; genetic robustness.
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