Genetic differentiation in the MAT-proximal region is not sufficient for suppressing recombination in Podospora anserina

Abstract

Recombination is advantageous over the long-term, as it allows efficient selection and purging deleterious mutations. Nevertheless, recombination suppression has repeatedly evolved in sex chromosomes and mating-type chromosomes. The evolutionary causes for recombination suppression and the proximal mechanisms preventing crossing overs are still poorly understood. Several hypotheses have recently been suggested based on theoretical models, and in particular, that divergence could accumulate neutrally around a sex-determining region and reduce recombination rates, a self-reinforcing process that could foster progressive extension of recombination suppression. The ascomycete fungus Podospora anserina is an excellent model for investigating these questions. A 0.8 Mb region around the mating-type locus is non-recombining, despite being collinear between the two mating types. This fungus is mostly selfing, so that strains are highly homozygous, except in the non-recombining region around the mating-type locus that displays differentiation between mating types. Here, we generated a mutant to test the hypothesis that sequence divergence alone is responsible for recombination cessation. We replaced the mat-idiomorph by the sequence of the mat+ idiomorph, to obtain a strain that is sexually compatible with the mat-reference strain and isogenic to this strain in the MAT-proximal region. Crosses showed that recombination was still suppressed in the MAT-proximal region in the mutant strains, indicating that other proximal mechanisms than inversions or mere sequence divergence are responsible for recombination suppression in this fungus. This finding suggests that selective mechanisms likely acted for suppressing recombination, as the neutral model does not seem to hold, at least in this fungus. ARTICLE SUMMARYIn many organisms, a non-recombining region is observed around the sex-determining locus. In the fungus Podospora anserina, recombination is suppressed within an 800kb region around the mating-type locus. In natural strains, the genome is isogenic between two mating-types, except in this region displaying heterozygosity. To determine if this heterozygosity can be responsible for the lack of recombination, compatible strains were engineered to be isogenic, including in the non-recombining region. Recombination inhibition persisted, indicating that mere sequence divergence does not cause recombination suppression. Our study provides an interesting insight on the molecular and evolutionary causes of recombination inhibition.