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      Contrasting evolutionary genome dynamics between domesticated and wild yeasts

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          Abstract

          Structural rearrangements have long been recognized as an important source of genetic variation with implications in phenotypic diversity and disease, yet their detailed evolutionary dynamics remain elusive. Here, we use long-read sequencing to generate end-to-end genome assemblies for 12 strains representing major subpopulations of the partially domesticated yeast Saccharomyces cerevisiae and its wild relative Saccharomyces paradoxus. These population-level high-quality genomes with comprehensive annotation allow for the first time a precise definition of chromosomal boundaries between cores and subtelomeres and a high-resolution view of evolutionary genome dynamics. In chromosomal cores, S. paradoxus exhibits faster accumulation of balanced rearrangements (inversions, reciprocal translocations and transpositions) whereas S. cerevisiae accumulates unbalanced rearrangements (novel insertions, deletions and duplications) more rapidly. In subtelomeres, both species show extensive interchromosomal reshuffling, with a higher tempo in S. cerevisiae. Such striking contrasts between wild and domesticated yeasts likely reflect the influence of human activities on structural genome evolution.

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          Most cited references63

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Structural variation in the human genome.

            The first wave of information from the analysis of the human genome revealed SNPs to be the main source of genetic and phenotypic human variation. However, the advent of genome-scanning technologies has now uncovered an unexpectedly large extent of what we term 'structural variation' in the human genome. This comprises microscopic and, more commonly, submicroscopic variants, which include deletions, duplications and large-scale copy-number variants - collectively termed copy-number variants or copy-number polymorphisms - as well as insertions, inversions and translocations. Rapidly accumulating evidence indicates that structural variants can comprise millions of nucleotides of heterogeneity within every genome, and are likely to make an important contribution to human diversity and disease susceptibility.
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              Population genomics of domestic and wild yeasts

              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.
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                Author and article information

                Journal
                9216904
                2419
                Nat Genet
                Nat. Genet.
                Nature genetics
                1061-4036
                1546-1718
                18 April 2017
                17 April 2017
                June 2017
                17 October 2017
                : 49
                : 6
                : 913-924
                Affiliations
                [1 ]Université Côte d'Azur, CNRS, INSERM, IRCAN, Nice, France
                [2 ]Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom
                [3 ]Department of Chemistry and Molecular Biology, Gothenburg University, Gothenburg 40530, Sweden
                [4 ]Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France
                Author notes
                [* ]Corresponding author: Gianni Liti ( gianni.liti@ 123456unice.fr )
                [+]

                Current address: Cancer Research UK Cambridge Institute, Li Ka Shing Centre, University of Cambridge, Cambridge CB2 0RE, United Kingdom.

                Article
                EMS72044
                10.1038/ng.3847
                5446901
                28416820
                1cb7b274-fc50-417a-9bf4-19c0cc852d62

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                Genetics
                Genetics

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