Population genomics of domestic and wild yeasts

Gianni Liti,Alan M Moses,Douda Bensasson,Stephen A James,David M Carter,Elizabeth Bailes,Edward J Louis,Alexander Van Oudenaarden,Austin Burt,Ian N Roberts,Ian Goodhead,Vassiliki Koufopanou,Richard Durbin,Robert P Davey,Leopold Parts,Alex N Nguyen,David B H Barton,Sarah Sims,Casey M Bergman,Jonas Warringer,Michael A Quail,Isheng Jason Tsai ,Michael O’kelly ,Frances J.d Smith ,Matthew C Jones

doi:10.1038/nature07743

Abstract

Since the completion of the genome sequence of Saccharomyces cerevisiae in 19961,2, there has been an exponential increase in complete genome sequences accompanied by great advances in our understanding of genome evolution. Although little is known about the natural and life histories of yeasts in the wild, there are an increasing number of studies looking at ecological and geographic distributions3,4, population structure5-8, and sexual versus asexual reproduction9,10. Less well understood at the whole genome level are the evolutionary processes acting within populations and species leading to adaptation to different environments, phenotypic differences and reproductive isolation. Here we present one- to four-fold or more coverage of the genome sequences of over seventy isolates of the baker's yeast, S. cerevisiae, and its closest relative, S. paradoxus. We examine variation in gene content, SNPs, indels, copy numbers and transposable elements. We find that phenotypic variation broadly correlates with global genome-wide phylogenetic relationships. Interestingly, S. paradoxus populations are well delineated along geographic boundaries while the variation among worldwide S. cerevisiae isolates shows less differentiation and is comparable to a single S. paradoxus population. Rather than one or two domestication events leading to the extant baker's yeasts, the population structure of S. cerevisiae consists of a few well-defined geographically isolated lineages and many different mosaics of these lineages, supporting the idea that human influence provided the opportunity for cross-breeding and production of new combinations of pre-existing variation.

Highlights

The S. cerevisiae population structure is more complex
Rather than one or two domestication events leading to the extant baker's yeasts, the population structure of S. cerevisiae consists of a few well-defined geographically isolated lineages and many different mosaics of these lineages, supporting the idea that human influence provided the opportunity for crossbreeding and production of new combinations of pre-existing variation
Much of the unplaced material is subtelomeric. This is in contrast to a genome-wide analysis of copy number based on the numbers of reads of each strain aligning to each gene in the reference sequence, which showed very little significant copy number variation (CNV) outside the rDNA region

Summary

Introduction

The S. cerevisiae population structure is more complex. There are five lineages that exhibit the same phylogenetic relationship across their entire genomes, which we consider to be ‘clean’ non-mosaic lineages (Fig. 1C). Rather than one or two domestication events leading to the extant baker's yeasts, the population structure of S. cerevisiae consists of a few well-defined geographically isolated lineages and many different mosaics of these lineages, supporting the idea that human influence provided the opportunity for crossbreeding and production of new combinations of pre-existing variation. We report nearly complete genome sequences of S. cerevisiae and S. paradoxus from a large variety of sources and locations (Table S1 and S2).

Results

Conclusion