Combinations of Spok genes create multiple meiotic drivers in Podospora

Abstract

Meiotic drive is the preferential transmission of a particular allele during sexual reproduction. The phenomenon is observed as spore killing in multiple fungi. In natural populations of Podospora anserina, seven spore killer types ( Psks) have been identified through classical genetic analyses. Here we show that the Spok gene family underlies the Psks. The combination of Spok genes at different chromosomal locations defines the spore killer types and creates a killing hierarchy within a population. We identify two novel Spok homologs located within a large (74–167 kbp) region (the Spok block) that resides in different chromosomal locations in different strains. We confirm that the SPOK protein performs both killing and resistance functions and show that these activities are dependent on distinct domains, a predicted nuclease and kinase domain. Genomic and phylogenetic analyses across ascomycetes suggest that the Spok genes disperse through cross-species transfer, and evolve by duplication and diversification within lineages.

eLife digest

In many organisms, most cells carry two versions of a given gene, one coming from the mother and the other from the father. An exception is sexual cells such as eggs, sperm, pollen or spores, which should only contain one variant of a gene. During their formation, these cells usually have an equal chance of inheriting one of the two gene versions.

However, a certain class of gene variants called meiotic drivers can cheat this process and end up in more than half of the sexual cells; often, the cells that contain the drivers can kill sibling cells that do not carry these variants. This results in the selfish genetic elements spreading through populations at a higher rate, sometimes with severe consequences such as shifting the ratio of males to females.

Meiotic drivers have been discovered in a wide range of organisms, from corn to mice to fruit flies and bread mold. They also exist in the fungus Podospora anserina, where they are called ‘spore killers’. Fungi are often used to study complex genetic processes, yet the identity and mode of action of spore killers in P. anserina were still unknown.

Vogan, Ament-Velásquez et al. used a combination of genetic methods to identify three genes from the Spok family which are responsible for certain spores being able to kill their siblings. Two of these were previously unknown, and they could be found in different locations throughout the genome as part of a larger genetic region. Depending on the combination of Spok genes it carries, a spore can kill or be protected against other spores that contain different permutations of the genes. Copies of these genes were also shown to be present in other fungi, including species that are a threat to crops.

Scientists have already started to create synthetic meiotic drivers to manipulate how certain traits are inherited within a population. This could be useful to control or eradicate pests and insects that transmit dangerous diseases. The results by Vogan, Ament-Velásquez et al. shine a light on the complex ways that natural meiotic drivers work, including how they can be shared between species; this knowledge could inform how to safely deploy synthetic drivers in the wild.