The roles of whole-genome and small-scale duplications in the functional specialization of Saccharomyces cerevisiae genes.
The roles of whole-genome and small-scale duplications in the functional specialization of Saccharomyces cerevisiae genes.
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DOI:
10.1371/journal.pgen.1003176
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发表时间:
2013
期刊:
影响因子:
4.5
通讯作者:
Jones GW
中科院分区:
文献类型:
--
作者:
Fares MA;Keane OM;Toft C;Carretero-Paulet L;Jones GW
Researchers have long been enthralled with the idea that gene duplication can generate novel functions, crediting this process with great evolutionary importance. Empirical data shows that whole-genome duplications (WGDs) are more likely to be retained than small-scale duplications (SSDs), though their relative contribution to the functional fate of duplicates remains unexplored. Using the map of genetic interactions and the re-sequencing of 27 Saccharomyces cerevisiae genomes evolving for 2,200 generations we show that SSD-duplicates lead to neo-functionalization while WGD-duplicates partition ancestral functions. This conclusion is supported by: (a) SSD-duplicates establish more genetic interactions than singletons and WGD-duplicates; (b) SSD-duplicates copies share more interaction-partners than WGD-duplicates copies; (c) WGD-duplicates interaction partners are more functionally related than SSD-duplicates partners; (d) SSD-duplicates gene copies are more functionally divergent from one another, while keeping more overlapping functions, and diverge in their sub-cellular locations more than WGD-duplicates copies; and (e) SSD-duplicates complement their functions to a greater extent than WGD–duplicates. We propose a novel model that uncovers the complexity of evolution after gene duplication. Gene duplication involves the doubling of a gene, originating an identical gene copy. Early evolutionary theory predicted that, as one gene copy is performing the ancestral function, the other gene copy, devoid from strong selection constraints, could evolve exploring alternative functions. Because of its potential to generate novel functions, hence biological complexity, gene duplication has been credited with enormous evolutionary importance. The way in which duplicated genes acquire novel functions remains the focus of intense research. Does the mechanism of duplication—duplication of small genome regions versus genome duplication—influence the fate of duplicates? Although it has been shown that the mechanism of duplication determines the persistence of genes in duplicate, a model describing the functional fates of duplicates generated by whole-genome or small-scale duplications remains largely obscure. Here we show that despite the large amount of genetic material originated by whole-genome duplication in the yeast Saccharomyces cerevisiae, these duplicates specialized in subsets of ancestral functions. Conversely, small-scale duplicates originated novel functions. We describe and test a model to explain the evolutionary dynamics of duplicates originated by different mechanisms. Our results shed light on the functional fates of duplicates and role of the duplication mechanism in generating functional diversity.
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