An introgressed gene causes meiotic drive inNeurospora sitophila

Abstract

Meiotic drive elements cause their own preferential transmission following meiosis. In fungi, this phenomenon takes the shape of spore killing, and in the filamentous ascomyceteNeurospora sitophila, theSk-1spore killer element is found in many natural populations. In this study, we identify the gene responsible for spore killing inSk-1by generating both long- and short-read genomic data and by using these data to perform a genome-wide association test. We name this geneSpk-1. Through molecular dissection, we show that a single 405-nt-long open reading frame generates a product that both acts as a poison capable of killing sibling spores and as an antidote that rescues spores that produce it. By phylogenetic analysis, we demonstrate that the gene has likely been introgressed from the closely related speciesNeurospora hispaniola, and we identify three subclades ofN. sitophila, one whereSk-1is fixed, another whereSk-1is absent, and a third where both killer and sensitive strain are found. Finally, we show that spore killing can be suppressed through an RNA interference-based genome defense pathway known as meiotic silencing by unpaired DNA.Spk-1is not related to other known meiotic drive genes, and similar sequences are only found withinNeurospora. These results shed light on the diversity of genes capable of causing meiotic drive, their origin and evolution, and their interaction with the host genome.