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

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.

Atypical meiosis can be adaptive in outcrossed Schizosaccharomyces pombe due to wtf meiotic drivers

“…We next wanted to determine why so many of the surviving spores produced by outcrossed S. pombe diploids were heterozygous disomes (aneuploids or diploids) for chromosome 3. We previously proposed a model in which distinct wtf meiotic drivers, which are nearly all on chromosome 3, were killing haploid spores ( López Hernández and Zanders, 2018 ; Zanders et al, 2014 ). We hypothesized that in the presence of diverged meiotic drivers on opposite haplotypes, haploid spores will inherit only one set of drivers and be killed by the drivers they do not inherit.…”

“…We have previously speculated that the wtf gene family specifically expanded on chromosome 3 and not on chromosomes 1 or 2 as aneuploid spores provide an avenue to mitigate the fitness costs of multiple drivers ( López Hernández and Zanders, 2018 ). The results of this study support and expand on that model.…”

The wtf4 meiotic driver utilizes controlled protein aggregation to generate selective cell death

“…The recently characterized wtf gene family of Schizosaccharomyces pombe includes several meiotic drivers ( Bravo Núñez et al, 2018a ; Eickbush et al, 2019 ; Hu et al, 2017 ; López Hernández and Zanders, 2018 ; Nuckolls et al, 2017 ). The wtf coding sequences are small (~1 kb) and encode autonomous drivers that specifically kill meiotic products (spores) that do not inherit the wtf + allele from wtf + / wtf - heterozygotes.…”

Atypical meiosis can be adaptive in outcrossedS. pombedue towtfmeiotic drivers

“…We next wanted to determine why so many of the surviving spores produced by outcrossed S. pombe diploids were heterozygous disomes for chromosome 3. We previously proposed a model in which distinct wtf meiotic drivers found on competing chromosome 3 haplotypes were killing haploid spores (López Hernández and Zanders 2018). We hypothesized that in the presence of diverged meiotic drivers on opposite haplotypes, haploid spores will inherit one driver and be killed by the driver on the opposite haplotype.…”

“…Importantly, an extra copy of chromosome 3 is the only aneuploidy tolerated in S. pombe (Niwa et al, 2006). We have previously speculated that the wtf gene family specifically expanded on chromosome 3 as aneuploid spores provide an avenue to mitigate the fitness costs of multiple drivers (López Hernández and Zanders 2018; Zanders et al, 2014). The results of this study support and expand on that model.…”