Abstract
We recently described the presence of large chromosomal segments resulting from independent horizontal gene transfer (HGT) events in the genome of Saccharomyces cerevisiae strains, mostly of wine origin. We report here evidence for the amplification of one of these segments, a 17 kb DNA segment from Zygosaccharomyces bailii, in the genome of S. cerevisiae strains. The copy number, organization and location of this region differ considerably between strains, indicating that the insertions are independent and that they are post-HGT events. We identified eight different forms in 28 S. cerevisiae strains, mostly of wine origin, with up to four different copies in a single strain. The organization of these forms and the identification of an autonomously replicating sequence functional in S. cerevisiae, strongly suggest that an extrachromosomal circular DNA (eccDNA) molecule serves as an intermediate in the amplification of the Z. bailii region in yeast genomes. We found little or no sequence similarity at the breakpoint regions, suggesting that the insertions may be mediated by nonhomologous recombination. The diversity between these regions in S. cerevisiae represents roughly one third the divergence among the genomes of wine strains, which confirms the recent origin of this event, posterior to the start of wine strain expansion. This is the first report of a circle-based mechanism for the expansion of a DNA segment, mediated by nonhomologous recombination, in natural yeast populations.
Highlights
The transfer of genetic information across normal mating barriers, known as horizontal or lateral gene transfer (HGT), has long been recognized as one of the major forces driving prokaryote evolution, but has generally been seen as more limited in eukaryotic genomes [1,2]
We looked for these three regions in the genome sequence of 59A, a haploid derivative of EC1118
Southern blot hybridization on the chromosomes of EC1118 confirmed that three copies of this region were present in EC1118: the copy initially described on chromosome XIV and two additional copies found in chromosomal bands attributed to chromosomes X and XII (Figure 2)
Summary
The transfer of genetic information across normal mating barriers, known as horizontal or lateral gene transfer (HGT), has long been recognized as one of the major forces driving prokaryote evolution, but has generally been seen as more limited in eukaryotic genomes [1,2]. Introgressions between closely related yeast species [8,9] or between varieties of the basidiomycete yeast Cryptococcus neoformans [10,11] have been described, suggesting that this mechanism is more widespread than previously thought in yeast genomes. The genome sequence of the commercial wine yeast strain EC1118 contains three gene clusters resulting from horizontal transfers [12], two of which are widespread among wine yeasts. The genes in these regions encode proteins involved in key metabolic functions during winemaking [12,13], strongly suggesting that HGT is one of the mechanisms by which wine yeast strains adapt to their high-sugar, low-nitrogen environment
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