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      Veni, vidi, vici: the success of wtf meiotic drivers in fission yeast

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          Abstract

          Meiotic drivers are selfish DNA loci that can bias their own transmission into gametes. Owing to their transmission advantages, meiotic drivers can spread in populations even if the drivers or linked variants decrease organismal fitness. Meiotic drive was first formally described in the 1950s and is thought to be a powerful force shaping eukaryotic genomes. Classic genetic analyses have detected the action of meiotic drivers in plants, filamentous fungi, insects and vertebrates. Several of these drive systems have limited experimental tractability and relatively little is known about the molecular mechanisms of meiotic drive. Recently, however, meiotic drivers were discovered in a yeast species. The Schizosaccharomyces pombe wtf gene family contains several active meiotic drive genes. This review summarizes what is known about the wtf family and highlights its potential as a highly tractable experimental model for molecular and evolutionary characterization of meiotic drive.

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          Most cited references32

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          Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast

          Large structural variations (SVs) within genomes are more challenging to identify than smaller genetic variants but may substantially contribute to phenotypic diversity and evolution. We analyse the effects of SVs on gene expression, quantitative traits and intrinsic reproductive isolation in the yeast Schizosaccharomyces pombe. We establish a high-quality curated catalogue of SVs in the genomes of a worldwide library of S. pombe strains, including duplications, deletions, inversions and translocations. We show that copy number variants (CNVs) show a variety of genetic signals consistent with rapid turnover. These transient CNVs produce stoichiometric effects on gene expression both within and outside the duplicated regions. CNVs make substantial contributions to quantitative traits, most notably intracellular amino acid concentrations, growth under stress and sugar utilization in winemaking, whereas rearrangements are strongly associated with reproductive isolation. Collectively, these findings have broad implications for evolution and for our understanding of quantitative traits including complex human diseases.
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            Comparative functional genomics of the fission yeasts.

            The fission yeast clade--comprising Schizosaccharomyces pombe, S. octosporus, S. cryophilus, and S. japonicus--occupies the basal branch of Ascomycete fungi and is an important model of eukaryote biology. A comparative annotation of these genomes identified a near extinction of transposons and the associated innovation of transposon-free centromeres. Expression analysis established that meiotic genes are subject to antisense transcription during vegetative growth, which suggests a mechanism for their tight regulation. In addition, trans-acting regulators control new genes within the context of expanded functional modules for meiosis and stress response. Differences in gene content and regulation also explain why, unlike the budding yeast of Saccharomycotina, fission yeasts cannot use ethanol as a primary carbon source. These analyses elucidate the genome structure and gene regulation of fission yeast and provide tools for investigation across the Schizosaccharomyces clade.
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              The Ecology and Evolutionary Dynamics of Meiotic Drive.

              Meiotic drivers are genetic variants that selfishly manipulate the production of gametes to increase their own rate of transmission, often to the detriment of the rest of the genome and the individual that carries them. This genomic conflict potentially occurs whenever a diploid organism produces a haploid stage, and can have profound evolutionary impacts on gametogenesis, fertility, individual behaviour, mating system, population survival, and reproductive isolation. Multiple research teams are developing artificial drive systems for pest control, utilising the transmission advantage of drive to alter or exterminate target species. Here, we review current knowledge of how natural drive systems function, how drivers spread through natural populations, and the factors that limit their invasion.
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                Author and article information

                Contributors
                sez@stowers.org
                Journal
                Yeast
                Yeast
                10.1002/(ISSN)1097-0061
                YEA
                Yeast (Chichester, England)
                John Wiley and Sons Inc. (Hoboken )
                0749-503X
                1097-0061
                21 February 2018
                July 2018
                : 35
                : 7 ( doiID: 10.1002/yea.v35.7 )
                : 447-453
                Affiliations
                [ 1 ] Stowers Institute for Medical Research Kansas City MO 64110 USA
                [ 2 ] Department of Molecular and Integrative Physiology University of Kansas Medical Center Kansas City KS 66160 USA
                Author notes
                [*] [* ] Correspondence

                Sarah E. Zanders, Stowers Institute for Medical Research, 1000 E 50th Street, Kansas City, Missouri 64110.

                Email: sez@ 123456stowers.org

                Author information
                http://orcid.org/0000-0003-1867-986X
                Article
                YEA3305 YEA-Oct-17-0158.R1
                10.1002/yea.3305
                6033644
                29322557
                ea2a57a7-a619-49a3-92e2-bf57aad00843
                © 2018 The Authors. Yeast published by John Wiley & Sons, Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 09 October 2017
                : 30 November 2017
                : 22 December 2017
                Page count
                Figures: 2, Tables: 0, Pages: 7, Words: 4217
                Funding
                Funded by: National Institute of General Medical Sciences
                Award ID: R00GM114436
                Funded by: Stowers Institute for Medical Research
                Categories
                Budding Topic
                Budding Topic
                Custom metadata
                2.0
                yea3305
                July 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.4.3 mode:remove_FC converted:23.07.2018

                Molecular biology
                infertility,meiosis,meitoic drive,schizosaccharomyces,speciation
                Molecular biology
                infertility, meiosis, meitoic drive, schizosaccharomyces, speciation

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