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.
Highlights
The genomes of all Eukaryotes harbor selfish genetic elements that employ a variety of mechanisms to undermine the canonical modes of DNA replication and meiosis in order to bias their own transmission (Werren et al, 1988; Burt and Trivers, 2009)
To investigate the genetic basis of spore killing in P. anserina, we generated high-quality wholegenome assemblies using a combination of long-read (PacBio and MinION Oxford Nanopore) and short-read (Illumina HiSeq) technologies
Through our integrative approach of genomics, molecular biology and phenotyping, we have been able to demonstrate that the multiple drive elements that have been genetically identified in P. anserina are not based on different underlying molecular mechanisms and/or specific gene interactions, but rather involve combinations of closely related driver genes that belong to the same Spok gene family
Summary
The genomes of all Eukaryotes harbor selfish genetic elements that employ a variety of mechanisms to undermine the canonical modes of DNA replication and meiosis in order to bias their own transmission (Werren et al, 1988; Burt and Trivers, 2009). One important class of selfish genetic elements are known as meiotic drivers These elements use a variety of mechanisms to hijack meiosis in order to bias their transmission to the gametes in proportions greater than 50% (Sandler and Novitski, 1957). This segregation distortion of alleles can be difficult to observe unless it is linked to an obvious phenotype such as sex (Sandler and Novitski, 1957; Helleu et al, 2014), the prevalence of meiotic drive in nature is probably underestimated. Spore killing is apparent in the sexual structures (asci) of the fungi because it results in half of the normal number
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