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Research article - Peer-reviewed, 2021

Sex without crossing over in the yeast Saccharomycodes ludwigii

Papaioannou, Ioannis A.; Dutreux, Fabien; Peltier, France A.; Maekawa, Hiromi; Delhomme, Nicolas; Bardhan, Amit; Friedrich, Anne; Schacherer, Joseph; Knop, Michael

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.

Keywords

Achiasmate meiosis; Automixis; Crossing over; Intratetrad mating; Meiotic recombination; Linkage disequilibrium; Mutation accumulation; Mutation rate; Saccharomycodes ludwigii

Published in

Genome Biology
2021, volume: 22, number: 1, article number: 303
Publisher: BMC

Authors' information

Papaioannou, Ioannis A.
Ruprecht Karls University Heidelberg
Dutreux, Fabien
Universites de Strasbourg Etablissements Associes
Peltier, France A.
Ruprecht Karls University Heidelberg
Maekawa, Hiromi
Kyushu University
Swedish University of Agricultural Sciences, Department of Forest Genetics and Plant Physiology
Bardhan, Amit
Ruprecht Karls University Heidelberg
Friedrich, Anne
Universites de Strasbourg Etablissements Associes
Schacherer, Joseph
Institut Universitaire de France
Knop, Michael
Ruprecht Karls University Heidelberg

UKÄ Subject classification

Microbiology

Publication Identifiers

DOI: https://doi.org/10.1186/s13059-021-02521-w

URI (permanent link to this page)

https://res.slu.se/id/publ/114341