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      Killer Meiotic Drive and Dynamic Evolution of the wtf Gene Family

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          Abstract

          Natural selection works best when the two alleles in a diploid organism are transmitted to offspring at equal frequencies. Despite this, selfish loci known as meiotic drivers that bias their own transmission into gametes are found throughout eukaryotes. Drive is thought to be a powerful evolutionary force, but empirical evolutionary analyses of drive systems are limited by low numbers of identified meiotic drive genes. Here, we analyze the evolution of the wtf gene family of Schizosaccharomyces pombe that contains both killer meiotic drive genes and suppressors of drive. We completed assemblies of all wtf genes for two S. pombe isolates, as well as a subset of wtf genes from over 50 isolates. We find that wtf copy number can vary greatly between isolates and that amino acid substitutions, expansions and contractions of DNA sequence repeats, and nonallelic gene conversion between family members all contribute to dynamic wtf gene evolution. This work demonstrates the power of meiotic drive to foster rapid evolution and identifies a recombination mechanism through which transposons can indirectly mobilize meiotic drivers.

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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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              PomBase: a comprehensive online resource for fission yeast

              PomBase (www.pombase.org) is a new model organism database established to provide access to comprehensive, accurate, and up-to-date molecular data and biological information for the fission yeast Schizosaccharomyces pombe to effectively support both exploratory and hypothesis-driven research. PomBase encompasses annotation of genomic sequence and features, comprehensive manual literature curation and genome-wide data sets, and supports sophisticated user-defined queries. The implementation of PomBase integrates a Chado relational database that houses manually curated data with Ensembl software that supports sequence-based annotation and web access. PomBase will provide user-friendly tools to promote curation by experts within the fission yeast community. This will make a key contribution to shaping its content and ensuring its comprehensiveness and long-term relevance.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Mol Biol Evol
                Mol. Biol. Evol
                molbev
                Molecular Biology and Evolution
                Oxford University Press
                0737-4038
                1537-1719
                June 2019
                16 April 2019
                16 April 2019
                : 36
                : 6
                : 1201-1214
                Affiliations
                [1 ]Stowers Institute for Medical Research, Kansas City, MO
                [2 ]Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA
                [3 ]Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, KS
                Author notes
                Corresponding author: E-mail: sez@ 123456stowers.org .
                Author information
                http://orcid.org/0000-0003-1867-986X
                Article
                msz052
                10.1093/molbev/msz052
                6526906
                30991417
                8bdfa66a-bacb-40c5-aa66-8d1e4d0ddfc0
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Pages: 14
                Funding
                Funded by: Stowers Institute for Medical Research 10.13039/100007795
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: R00GM114436
                Award ID: DP2GM132936
                Award ID: R01GM074108
                Categories
                Discoveries

                Molecular biology
                meiotic drive,gene conversion,genetic conflict,recombination,rapid evolution,meiosis
                Molecular biology
                meiotic drive, gene conversion, genetic conflict, recombination, rapid evolution, meiosis

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