Recurrent Rearrangement during Adaptive Evolution in an Interspecific Yeast Hybrid Suggests a Model for Rapid Introgression
| Autor: | Terry Paulish, Jeff S. Piotrowski, Edward J. Louis, Evgueny Kroll, Gregory Koniges, Gianni Liti, Alison Stanbery, Barbara Dunn, Gavin Sherlock, Frank Rosenzweig |
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| Jazyk: | angličtina |
| Rok vydání: | 2013 |
| Předmět: |
Evolutionary Genetics
Cancer Research Chromosomal translocation Yeast and Fungal Models Genome Microbial Physiology Gene Expression Regulation Fungal Natural Selection Genome Sequencing Genome Evolution Cation Transport Proteins Genetics (clinical) 2. Zero hunger Genetics 0303 health sciences biology Chromosome Biology Microbial Mutation Genomics Biological Evolution Chromosomes Fungal Genome Fungal Research Article Genome evolution Chromosome Structure and Function Evolutionary Processes Saccharomyces cerevisiae Proteins lcsh:QH426-470 Saccharomyces cerevisiae Introgression Forms of Evolution Microbiology 03 medical and health sciences Model Organisms Species Specificity Genetic Mutation Molecular Biology Gene Biology Ecology Evolution Behavior and Systematics 030304 developmental biology Synteny Evolutionary Biology 030306 microbiology Mutation Types Chromosome Genomic Evolution biology.organism_classification Quaternary Ammonium Compounds lcsh:Genetics Microbial Evolution Hybridization Genetic Population Genetics |
| Zdroj: | PLoS Genetics PLoS Genetics, Vol 9, Iss 3, p e1003366 (2013) |
| ISSN: | 1553-7404 1553-7390 |
| Popis: | Genome rearrangements are associated with eukaryotic evolutionary processes ranging from tumorigenesis to speciation. Rearrangements are especially common following interspecific hybridization, and some of these could be expected to have strong selective value. To test this expectation we created de novo interspecific yeast hybrids between two diverged but largely syntenic Saccharomyces species, S. cerevisiae and S. uvarum, then experimentally evolved them under continuous ammonium limitation. We discovered that a characteristic interspecific genome rearrangement arose multiple times in independently evolved populations. We uncovered nine different breakpoints, all occurring in a narrow ∼1-kb region of chromosome 14, and all producing an “interspecific fusion junction” within the MEP2 gene coding sequence, such that the 5′ portion derives from S. cerevisiae and the 3′ portion derives from S. uvarum. In most cases the rearrangements altered both chromosomes, resulting in what can be considered to be an introgression of a several-kb region of S. uvarum into an otherwise intact S. cerevisiae chromosome 14, while the homeologous S. uvarum chromosome 14 experienced an interspecific reciprocal translocation at the same breakpoint within MEP2, yielding a chimaeric chromosome; these events result in the presence in the cell of two MEP2 fusion genes having identical breakpoints. Given that MEP2 encodes for a high-affinity ammonium permease, that MEP2 fusion genes arise repeatedly under ammonium-limitation, and that three independent evolved isolates carrying MEP2 fusion genes are each more fit than their common ancestor, the novel MEP2 fusion genes are very likely adaptive under ammonium limitation. Our results suggest that, when homoploid hybrids form, the admixture of two genomes enables swift and otherwise unavailable evolutionary innovations. Furthermore, the architecture of the MEP2 rearrangement suggests a model for rapid introgression, a phenomenon seen in numerous eukaryotic phyla, that does not require repeated backcrossing to one of the parental species. Author Summary Interspecific hybridization occurs when two different species mate and produce viable offspring. While hybrid offspring are usually sterile, like the mule, which results from a horse–donkey mating, sometimes they are fertile, creating new species. Indeed, many plant and animal species have arisen via this mechanism. Because interspecific hybridization occurs between different yeast species, and because they are such tractable models, yeast are ideally suited for experimentally investigating the genomic consequences of interspecific hybridization. We created an interspecific yeast hybrid by crossing S. cerevisiae and S. uvarum, and then studied genomic changes that occurred as it adaptively evolved in a stressful nitrogen-limiting environment. We discovered that a characteristic rearrangement between the parental species' chromosomes evolved independently many times, and always within a particular gene encoding a protein that imports nitrogen into the cell. Evolved hybrids carrying this rearrangement grew faster under nitrogen-limitation than ancestral hybrids, suggesting that the rearrangement is beneficial in nitrogen-poor environments. Our results suggest that having the genomes of two different species within a cell provides novel sources of variation for evolution to act upon, leading to adaptations that could not occur in either parental species. |
| Databáze: | OpenAIRE |
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