title: Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression.
abstract: 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.
authors.affiliation: Department of Genetics, Stanford University School of Medicine, Stanford, California, United States of America.
authors.forename: Barbara
authors.initials: B
authors.lastname: Dunn
authors.forename: Terry
authors.initials: T
authors.lastname: Paulish
authors.forename: Alison
authors.initials: A
authors.lastname: Stanbery
authors.forename: Jeff
authors.initials: J
authors.lastname: Piotrowski
authors.forename: Gregory
authors.initials: G
authors.lastname: Koniges
authors.forename: Evgueny
authors.initials: E
authors.lastname: Kroll
authors.forename: Edward J
authors.initials: EJ
authors.lastname: Louis
authors.forename: Gianni
authors.initials: G
authors.lastname: Liti
authors.forename: Gavin
authors.initials: G
authors.lastname: Sherlock
authors.forename: Frank
authors.initials: F
authors.lastname: Rosenzweig
mesh_terms: D005075:Biological Evolution; D027682:Cation Transport Proteins / Q000235:genetics*; D015825:Chromosomes, Fungal / Q000235:genetics*; D015966:Gene Expression Regulation, Fungal; D016681:Genome, Fungal; D006824:Hybridization, Genetic; D000644:Quaternary Ammonium Compounds / Q000378:metabolism; D012441:Saccharomyces cerevisiae / Q000235:genetics*; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics*; D013045:Species Specificity
chemical_list: D027682:Cation Transport Proteins; C107270:MEP2 protein, S cerevisiae; D000644:Quaternary Ammonium Compounds; D029701:Saccharomyces cerevisiae Proteins
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