The Roles of Whole-Genome and Small-Scale Duplications in the Functional Specialization of Saccharomyces cerevisiae Genes (original) (raw)
Related papers
Pervasive and persistent redundancy among duplicated genes in yeast
PLoS genetics, 2008
The loss of functional redundancy is the key process in the evolution of duplicated genes. Here we systematically assess the extent of functional redundancy among a large set of duplicated genes in Saccharomyces cerevisiae. We quantify growth rate in rich medium for a large number of S. cerevisiae strains that carry single and double deletions of duplicated and singleton genes. We demonstrate that duplicated genes can maintain substantial redundancy for extensive periods of time following duplication (,100 million years). We find high levels of redundancy among genes duplicated both via the whole genome duplication and via smaller scale duplications. Further, we see no evidence that two duplicated genes together contribute to fitness in rich medium substantially beyond that of their ancestral progenitor gene. We argue that duplicate genes do not often evolve to behave like singleton genes even after very long periods of time.
Genomic Background Predicts the Fate of Duplicated Genes: Evidence From the Yeast Genome
Genetics, 2004
Gene duplication with subsequent divergence plays a central role in the acquisition of genes with novel function and complexity during the course of evolution. With reduced functional constraints or through positive selection, these duplicated genes may experience accelerated evolution. Under the model of subfunctionalization, loss of subfunctions leads to complementary acceleration at sites with two copies, and the difference in average rate between the sequences may not be obvious. On the other hand, the classical model of neofunctionalization predicts that the evolutionary rate in one of the two duplicates is accelerated. However, the classical model does not tell which of the duplicates experiences the acceleration in evolutionary rate. Here, we present evidence from the Saccharomyces cerevisiae genome that a duplicate located in a genomic region with a low-recombination rate is likely to evolve faster than a duplicate in an area of high recombination. This observation is consistent with population genetics theory that predicts that purifying selection is less effective in genomic regions of low recombination (Hill-Robertson effect). Together with previous studies, our results suggest the genomic background (e.g., local recombination rate) as a potential force to drive the divergence between nontandemly duplicated genes. This implies the importance of structure and complexity of genomes in the diversification of organisms via gene duplications.
Genetic interactions reveal the evolutionary trajectories of duplicate genes
Molecular Systems Biology, 2010
The characterization of functional redundancy and divergence between duplicate genes is an important step in understanding the evolution of genetic systems. Large-scale genetic network analysis in Saccharomyces cerevisiae provides a powerful perspective for addressing these questions through quantitative measurements of genetic interactions between pairs of duplicated genes, and more generally, through the study of genome-wide genetic interaction profiles associated with duplicated genes. We show that duplicate genes exhibit fewer genetic interactions than other genes because they tend to buffer one another functionally, whereas observed interactions are nonoverlapping and reflect their divergent roles. We also show that duplicate gene pairs are highly imbalanced in their number of genetic interactions with other genes, a pattern that appears to result from asymmetric evolution, such that one duplicate evolves or degrades faster than the other and often becomes functionally or conditionally specialized. The differences in genetic interactions are predictive of differences in several other evolutionary and physiological properties of duplicate pairs.
Gene and genome duplication are the major sources of biological innovations in plants and animals. Functional and transcriptional divergence between the copies after gene duplication has been considered the main driver of innovations. However, here we show that increased phenotypic plasticity after duplication plays a more major role than thought before in the origin of adaptations. We perform an exhaustive analysis of the transcriptional alterations of duplicated genes in the unicellular eukaryote Sac-charomyces cerevisiae when challenged with five different environmental stresses. Analysis of the tran-scriptomes of yeast shows that gene duplication increases the transcriptional response to environmental changes, with duplicated genes exhibiting signatures of adaptive transcriptional patterns in response to stress. The mechanism of duplication matters, with whole-genome duplicates being more transcriptionally altered than small-scale duplicates. The predominant transcriptional pattern follows the classic theory of evolution by gene duplication; with one gene copy remaining unaltered under stress, while its sister copy presents large transcriptional plasticity and a prominent role in adaptation. Moreover, we find additional transcriptional profiles that are suggestive of neo-and subfunctionalization of duplicate gene copies. These patterns are strongly correlated with the functional dependencies and sequence divergence profiles of gene copies. We show that, unlike singletons, duplicates respond more specifically to stress, supporting the role of natural selection in the transcriptional plasticity of duplicates. Our results reveal the underlying transcriptional complexity of duplicated genes and its role in the origin of adaptations.
Loss of protein interactions and regulatory divergence in yeast whole-genome duplicates
Genomics, 2009
Whole-genome duplications are important for the growth of genome complexity. We investigated various factors involved in the evolution of yeast whole-genome duplicates (ohnologs) making emphasis on the analysis of protein interactions. We found that ohnologs have a lower number of protein interactions compared with small-scale duplicates and singletons (by about − 40%). The loss of interactions was proportional to their initial number and independent of ohnolog position in the protein interaction network. A faster evolving member of an ohnolog pair has a lower number of interactions compared to its counterpart. The Gene Ontology mapping of non-overlapping and overlapping interactants of paired ohnologs reveals a sharp asymmetry in GO terms related to regulation. The fraction of these terms is much higher in nonoverlapping interactants (compared to overlapping interactants and total dataset). Network clustering coefficient is lower in ohnologs, yet they show an increased density of protein interactions restricted within the whole ohnologs set. These facts suggest that subfunctionalization (or subneofunctionalization) reflected in the loss of protein interactions was a prevailing process in the divergence of ohnologs, which distinguishes them from small-scale duplicates. The loss of protein interactions was associated with the regulatory divergence between the members of an ohnolog pair. A small-scale modularity (reflected in clustering coefficient) probably was not important for ohnologs retention, yet a larger-scale modularity could be involved in their evolution.
Genome research, 2014
Biological systems remain robust against certain genetic and environmental challenges. Robustness allows the exploration of ecological adaptations. It is unclear what factors contribute to increasing robustness. Gene duplication has been considered to increase genetic robustness through functional redundancy, accelerating the evolution of novel functions. However, recent findings have questioned the link between duplication and robustness. In particular, it remains elusive whether ancient duplicates still bear potential for innovation through preserved redundancy and robustness. Here we have investigated this question by evolving the yeast Saccharomyces cerevisiae for 2200 generations under conditions allowing the accumulation of deleterious mutations, and we put mechanisms of mutational robustness to a test. S. cerevisiae declined in fitness along the evolution experiment, but this decline decelerated in later passages, suggesting functional compensation of mutated genes. We resequ...
created by whole-genome duplication in yeast
Identification of orthologous genes across species becomes challenging in the presence of a whole genome duplication (WGD). We present a probabilistic method for identifying orthologs that considers all possible orthology/paralogy assignments for a set of genomes with a shared WGD (here five yeast species). This approach allows us to estimate how confident we can be in the orthology assignments in each genomic region.
Genome Biology, 2009
Background The direct examination of large, unbiased samples of young gene duplicates in their early stages of evolution is crucial to understanding the origin, divergence and preservation of new genes. Furthermore, comparative analysis of multiple genomes is necessary to determine whether patterns of gene duplication can be generalized across diverse lineages or are species-specific. Here we present results from an analysis comprising 68 duplication events in the Saccharomyces cerevisiae genome. We partition the yeast duplicates into ohnologs (generated by a whole-genome duplication) and non-ohnologs (from small-scale duplication events) to determine whether their disparate origins commit them to divergent evolutionary trajectories and genomic attributes. Results We conclude that, for the most part, ohnologs tend to appear remarkably similar to non-ohnologs in their structural attributes (specifically the relative composition frequencies of complete, partial and chimeric duplicates), the discernible length of the duplicated region (duplication span) as well as genomic location. Furthermore, we find notable differences in the features of S. cerevisiae gene duplicates relative to those of another eukaryote, Caenorhabditis elegans, with respect to chromosomal location, extent of duplication and the relative frequencies of complete, partial and chimeric duplications. Conclusions We conclude that the variation between yeast and worm duplicates can be attributed to differing mechanisms of duplication in conjunction with the varying efficacy of natural selection in these two genomes as dictated by their disparate effective population sizes.
Do disparate mechanisms of duplication add similar genes to the genome?
Trends in Genetics, 2005
Gene duplication is the fundamental source of new genes. Biases in duplication have profound implications for the dynamics of gene content during evolution. In this article, we compare genes arising from whole gene duplication (WGD), smaller scale duplication (SSD) and singletons in Saccharomyces cerevisiae. Our results demonstrate that genes duplicated by WGD and SSD are similarly biased with respect to codon bias and evolutionary rate, although differing significantly in their functional constituency.