A large gene family in fission yeast encodes spore killers that subvert Mendel’s law

Abstract

Spore killers in fungi are selfish genetic elements that distort Mendelian segregation in their favor. It remains unclear how many species harbor them and how diverse their mechanisms are. Here, we discover two spore killers from a natural isolate of the fission yeast Schizosaccharomyces pombe. Both killers belong to the previously uncharacterized wtf gene family with 25 members in the reference genome. These two killers act in strain-background-independent and genome-location-independent manners to perturb the maturation of spores not inheriting them. Spores carrying one killer are protected from its killing effect but not that of the other killer. The killing and protecting activities can be uncoupled by mutation. The numbers and sequences of wtf genes vary considerably between S. pombe isolates, indicating rapid divergence. We propose that wtf genes contribute to the extensive intraspecific reproductive isolation in S. pombe, and represent ideal models for understanding how segregation-distorting elements act and evolve.DOI: http://dx.doi.org/10.7554/eLife.26057.001

wtf genes are prolific dual poison-antidote meiotic drivers

“…Additionally, Hu et al, 2017 also identified two different wtf drivers in another Sp isolate (CBS5557) and both have a potential alternate start codon in exon 2. Of the 25 wtf loci in Sp , four ( wtf4 , wtf13 , wtf19 and wtf23 ) also appear to be capable of encoding two proteins and we predict these are active drive genes.…”

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

“…Hu et al found that gamete killing meiotic drive also contributed to infertility in the laboratory S. pombe /CBS5557 hybrids. They also identified two meiotic drive loci on chromosome 3 of CBS5557 (Hu et al, ).…”

“…Both groups identified distinct meiotic drive genes that are members of the previously uncharacterized wtf gene family. The S. kambucha genes were named wtf4 and wtf28 , whereas the CBS5557 genes were called cw9 and cw27 (Hu et al, ; Nuckolls et al, ). The wtf gene family owes its catchy name to the family's association with long terminal repeats (LTRs) of the Tf transposons (with Tf transposon).…”

“…The wtf gene family owes its catchy name to the family's association with long terminal repeats (LTRs) of the Tf transposons (with Tf transposon). Hu et al () demonstrated that this LTR association is not functionally important by showing that both cw9 and cw27 caused drive when their flanking LTRs were deleted.…”

“…Spore death and allele transmission bias are not observed in homozygotes ( wtf+ or wtf− ). All four described genes can cause drive when introduced to an ectopic locus in the laboratory S. pombe , indicating that they are each self‐sufficient for executing drive (Hu et al, ; Nuckolls et al, ). This is similar to other described single‐gene drive systems, het‐s and the Spok genes, of the Podospora anserina fungus (Dalstra et al, ; Grognet, Lalucque, Malagnac, & Silar, ).…”