Sex without crossing over in the yeast Saccharomycodes ludwigii

Abstract Background Intermixing of genomes through meiotic reassortment and recombination of homologous chromosomes is a unifying theme of sexual reproduction in eukaryotic organisms and is considered crucial for their adaptive evolution. Previous studies of the budding yeast species Saccharomycodes...

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Autores principales:	Ioannis A. Papaioannou, Fabien Dutreux, France A. Peltier, Hiromi Maekawa, Nicolas Delhomme, Amit Bardhan, Anne Friedrich, Joseph Schacherer, Michael Knop
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Achiasmate meiosis Automixis Crossing over Intratetrad mating Meiotic recombination Linkage disequilibrium Biology (General) QH301-705.5 Genetics QH426-470
Acceso en línea:	https://doaj.org/article/ff0e5dddea7246599fa1731d60cc9a30
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spelling	oai:doaj.org-article:ff0e5dddea7246599fa1731d60cc9a302021-11-08T11:17:18ZSex without crossing over in the yeast Saccharomycodes ludwigii10.1186/s13059-021-02521-w1474-760Xhttps://doaj.org/article/ff0e5dddea7246599fa1731d60cc9a302021-11-01T00:00:00Zhttps://doi.org/10.1186/s13059-021-02521-whttps://doaj.org/toc/1474-760XAbstract Background Intermixing of genomes through meiotic reassortment and recombination of homologous chromosomes is a unifying theme of sexual reproduction in eukaryotic organisms and is considered crucial for their adaptive evolution. Previous studies of the budding yeast species Saccharomycodes ludwigii suggested that meiotic crossing over might be absent from its sexual life cycle, which is predominated by fertilization within the meiotic tetrad. Results We demonstrate that recombination is extremely suppressed during meiosis in Sd. ludwigii. DNA double-strand break formation by the conserved transesterase Spo11, processing and repair involving interhomolog interactions are required for normal meiosis but do not lead to crossing over. Although the species has retained an intact meiotic gene repertoire, genetic and population analyses suggest the exceptionally rare occurrence of meiotic crossovers in its genome. A strong AT bias of spontaneous mutations and the absence of recombination are likely responsible for its unusually low genomic GC level. Conclusions Sd. ludwigii has followed a unique evolutionary trajectory that possibly derives fitness benefits from the combination of frequent mating between products of the same meiotic event with the extreme suppression of meiotic recombination. This life style ensures preservation of heterozygosity throughout its genome and may enable the species to adapt to its environment and survive with only minimal levels of rare meiotic recombination. We propose Sd. ludwigii as an excellent natural forum for the study of genome evolution and recombination rates.Ioannis A. PapaioannouFabien DutreuxFrance A. PeltierHiromi MaekawaNicolas DelhommeAmit BardhanAnne FriedrichJoseph SchachererMichael KnopBMCarticleAchiasmate meiosisAutomixisCrossing overIntratetrad matingMeiotic recombinationLinkage disequilibriumBiology (General)QH301-705.5GeneticsQH426-470ENGenome Biology, Vol 22, Iss 1, Pp 1-28 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Achiasmate meiosis Automixis Crossing over Intratetrad mating Meiotic recombination Linkage disequilibrium Biology (General) QH301-705.5 Genetics QH426-470
spellingShingle	Achiasmate meiosis Automixis Crossing over Intratetrad mating Meiotic recombination Linkage disequilibrium Biology (General) QH301-705.5 Genetics QH426-470 Ioannis A. Papaioannou Fabien Dutreux France A. Peltier Hiromi Maekawa Nicolas Delhomme Amit Bardhan Anne Friedrich Joseph Schacherer Michael Knop Sex without crossing over in the yeast Saccharomycodes ludwigii
description	Abstract Background Intermixing of genomes through meiotic reassortment and recombination of homologous chromosomes is a unifying theme of sexual reproduction in eukaryotic organisms and is considered crucial for their adaptive evolution. Previous studies of the budding yeast species Saccharomycodes ludwigii suggested that meiotic crossing over might be absent from its sexual life cycle, which is predominated by fertilization within the meiotic tetrad. Results We demonstrate that recombination is extremely suppressed during meiosis in Sd. ludwigii. DNA double-strand break formation by the conserved transesterase Spo11, processing and repair involving interhomolog interactions are required for normal meiosis but do not lead to crossing over. Although the species has retained an intact meiotic gene repertoire, genetic and population analyses suggest the exceptionally rare occurrence of meiotic crossovers in its genome. A strong AT bias of spontaneous mutations and the absence of recombination are likely responsible for its unusually low genomic GC level. Conclusions Sd. ludwigii has followed a unique evolutionary trajectory that possibly derives fitness benefits from the combination of frequent mating between products of the same meiotic event with the extreme suppression of meiotic recombination. This life style ensures preservation of heterozygosity throughout its genome and may enable the species to adapt to its environment and survive with only minimal levels of rare meiotic recombination. We propose Sd. ludwigii as an excellent natural forum for the study of genome evolution and recombination rates.
format	article
author	Ioannis A. Papaioannou Fabien Dutreux France A. Peltier Hiromi Maekawa Nicolas Delhomme Amit Bardhan Anne Friedrich Joseph Schacherer Michael Knop
author_facet	Ioannis A. Papaioannou Fabien Dutreux France A. Peltier Hiromi Maekawa Nicolas Delhomme Amit Bardhan Anne Friedrich Joseph Schacherer Michael Knop
author_sort	Ioannis A. Papaioannou
title	Sex without crossing over in the yeast Saccharomycodes ludwigii
title_short	Sex without crossing over in the yeast Saccharomycodes ludwigii
title_full	Sex without crossing over in the yeast Saccharomycodes ludwigii
title_fullStr	Sex without crossing over in the yeast Saccharomycodes ludwigii
title_full_unstemmed	Sex without crossing over in the yeast Saccharomycodes ludwigii
title_sort	sex without crossing over in the yeast saccharomycodes ludwigii
publisher	BMC
publishDate	2021
url	https://doaj.org/article/ff0e5dddea7246599fa1731d60cc9a30
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Sex without crossing over in the yeast Saccharomycodes ludwigii

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