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.

A Large Set of Newly Created Interspecific Saccharomyces Hybrids Increases Aromatic Diversity in Lager Beers

“…the genomes of interspecific hybrids originating from the same parents can stabilize differently, resulting in different genomic configurations, as reported in previous studies targeting interspecific hybrids (30,32,44,45). Newly developed interspecific hybrids show a broad temperature tolerance range.…”

“…Prior to phenotypic characterization, the genomes of the newly developed hybrids were therefore stabilized by growing interspecific hybrids for approximately 70 generations in industrial lager beer medium (see Materials and Methods for details). This number is shown to be sufficient to stabilize the genomes of newly formed interspecific yeast hybrids within the Saccharomyces genus (29)(30)(31)(32). Genetic stability was confirmed by genetic fingerprinting, and hybrids were considered stable when, after stabilization, both the interdelta and R3-RAPD band patterns were identical for the four biological replicates tested (see Fig.…”

“…Previous research showed that newly formed interspecific hybrid genomes are characterized by high plasticity and that genome rearrangements, such as whole or partial chromosome losses and introgressions, are common and can be directed by the environmental stress conditions applied (30,31,44,45). For example Dunn and coworkers (30) showed that newly formed interspecific hybrids between S. cerevisiae and S. uvarum exhibited a characteristic genome rearrangement pattern when hybrids were grown under continuous ammonium limitations (30).…”

“…The development of interspecific hybrids has proven to be a powerful approach to generate novel yeast variants with enhanced characteristics for wine making. Typically, an industrial strain of S. cerevisiae yeast is crossed with a wild, non-cerevisiae member of the Saccharomyces sensu stricto group, such as S. bayanus (15,(25)(26)(27), S. kudriavzevii (28,29), S. uvarum (30,31), or S. mikatae (32).…”

Rare Variants in Hypermutable Genes Underlie Common Morphology and Growth Traits in WildSaccharomyces paradoxus

“…Toward this end, hundreds of studies have sought to map causal genes, using tests for allele sharing among affected but unrelated individuals. Against a backdrop of recent successes in fruit fly and plant populations (Atwell et al 2010;Brachi et al 2010;Chan et al 2011;Filiault and Maloof 2012;Mackay et al 2012;Magwire et al 2012;Weber et al 2012;Dunn et al 2013), association mapping in many systems has yielded loci that explain only a small part of the variation in a given trait across individuals (McCarthy et al 2008). The latter challenges have motivated the proposal that the bulk of common phenotypic variation may be attributable to rare, highly penetrant mutations (Dickson et al 2010;McClellan and King 2010; Veltman and Brunner 2012), including recurrent variation at hypermutable loci (Shen et al 1996;Chan et al 2010;Michaelson et al 2012).…”