The Enterprise, a massive transposon carrying Spok meiotic drive genes

Abstract

The genomes of eukaryotes are full of parasitic sequences known as transposable elements (TEs). Here, we report the discovery of a putative giant tyrosine-recombinase-mobilized DNA transposon, Enterprise, from the model fungus Podospora anserina. Previously, we described a large genomic feature called the Spok block which is notable due to the presence of meiotic drive genes of the Spok gene family. The Spok block ranges from 110 kb to 247 kb and can be present in at least four different genomic locations within P. anserina, despite what is an otherwise highly conserved genome structure. We propose that the reason for its varying positions is that the Spok block is not only capable of meiotic drive but is also capable of transposition. More precisely, the Spok block represents a unique case where the Enterprise has captured the Spoks, thereby parasitizing a resident genomic parasite to become a genomic hyperparasite. Furthermore, we demonstrate that Enterprise (without the Spoks) is found in other fungal lineages, where it can be as large as 70 kb. Lastly, we provide experimental evidence that the Spok block is deleterious, with detrimental effects on spore production in strains which carry it. This union of meiotic drivers and a transposon has created a selfish element of impressive size in Podospora, challenging our perception of how TEs influence genome evolution and broadening the horizons in terms of what the upper limit of transposition may be.

A devil's bargain with transposable elements in plant pathogens

“…Fungi are excellent models to study TE dynamics because of their compact genomes. This is highlighted by the recent discovery of a massive transposon that shuttles meiotic drive genes around the genome in Podospora anserina [20]. New TE insertions in fission yeasts underlie the evolutionary dynamics of tolerance to environmental stressors [21].…”

Diverse mating phenotypes impact the spread of wtf meiotic drivers in Schizosaccharomyces pombe

“…We compared our data to a model in which driver heterozygotes have a fitness of 0.51, but we also considered variants of the model in which heterozygotes have fitness greater than 0.5, as can occur with spore killers in Podospora anserina ( Vogan et al, 2021 ; Martinossi-Allibert et al, 2021 ). In S. pombe , an increase in driver heterozygote fitness could occur if the driving alleles benefit from drive beyond the benefits gained directly by killing spores bearing the alternate allele.…”

“…As inbreeding is thought to inhibit the spread of selfish genes like drivers, drivers are predicted to be unsuccessful in species that rarely outcross ( Burt and Trivers, 1998 ; Hurst and Werren, 2001 ). This assumption appears to be challenged in several fungal species, including the fission yeast Schizosaccharomyces pombe ( Grognet et al, 2014 ; Hammond et al, 2012 ; Svedberg et al, 2021 ; van der Gaag et al, 2000 ; Vogan et al, 2021 ).…”

Red queen’s race: rapid evolutionary dynamics of an expanding family of meiotic drive factors and their hpRNA suppressors

“…These principles may apply more generally. Similar to the rapid amplification of Dox superfamily genes, and their association with 359 satellite repeats, recent findings from meiotic drive families across a range of non-Drosophila species recapitulate two broad themes: (1) ampliconic nature of drive loci, for example Slx/Sly in mice (Cocquet et al, 2012;Cocquet et al, 2010;Moretti et al, 2020), Spok meiotic drive gene family in Podospora anserina (Vogan et al, 2019), and the wtf meiotic drive gene family in S. pombe and certain other yeasts (Hu et al, 2017;Nuckolls et al, 2017), and (2) association of meiotic drive gene family expansion with repetitive elements, for instance, the expansions of Spok family genes mediated by Enterpriseclass transposable elements (Vogan et al, 2021).…”