In the filamentous fungus Podospora anserina, two phenomena are associated with polymorphism at the het-s locus, vegetative incompatibility and ascospore abortion. Two het-s alleles occur naturally, het-s and het-S. The het-s encoded protein is a prion propagating as a self-perpetuating amyloid aggregate. M eiotic drive is a process mediated by genetic elements, called segregation distorters, that actively bias Mendelian segregation in their favor. In metazoans, classic examples of meiotic drive include the t haplotype in mice and Segregation Distorter (SD) in Drosophila (1). In both these autosomal drive systems, heterozygous males produce gametes of the driver genotype in excess. The molecular mechanisms of meiotic drive remain largely elusive, except in the case of SD in Drosophila, where distortion involves a truncated form of a RanGAP protein and its mislocalization to the nucleus (2). The best studied examples of segregation distortion in fungi are the spore killer systems in the ascomycetes Neurospora crassa (3-6) and Podospora anserina (7). In these haploid organisms, the sexual progeny, the ascospores, are linearly arranged after meiosis. Ascomycetes therefore provide excellent opportunities to investigate the behavior of meiotic drive elements (8). Presence of a killer gene can readily be detected by directly analyzing the pattern of ascospore abortion. Spore killer genes exist as a killer and a sensitive allele or haplotype. In a killer ϫ sensitive cross, the ascospores harboring only the sensitive genotype degenerate. Heterokaryotic spores, containing both a sensitive and a killer nucleus, escape abortion. Both in Neurospora and in Podospora, several spore killer loci have been genetically identified, but so far the mechanism of spore killing is unknown.In 1965, Bernet (9, 10) described properties of the het-s gene in Podospora, now recognized to be analogous to a spore killer locus. The discovery that het-s encodes a prion protein (11, 12) places this observation into a new perspective. The het-s locus, together with at least eight other loci, determines vegetative incompatibility in P. anserina (13,14). Two alleles are found at this locus, termed het-s During the sexual cycle, a single mating-type culture of P. anserina differentiates both male (microconidia) and female (protoperithecia) reproductive structures. The protoperithecium emits a specialized hypha called the trichogyne. Fertilization occurs when a microconidium fuses with a trichogyne of opposite mating type. After migration of the male nucleus down the trichogyne into the female ascogonium, individualized male and female nuclei divide synchronously in a syncytial structure. Because the male gamete contributes very little cytoplasm to this heterokaryon, the cytoplasm of the zygote is essentially of maternal origin. Nuclei of opposite mating type then pair up, and karyogamy takes place in specialized cells. Importantly, at this stage there is a transition from a syncytial to a cellular state (21). Meiotic progeny are linearly arranged as ...

Prions are infectious proteins that cause fatal diseases in mammals. Prions have also been found in fungi, but studies on their role in nature are scarce. The proposed biological function of fungal prions is debated and varies from detrimental to benign or even beneficial. [Het-s] is a prion of the fungus Podospora anserina. The het-s locus exists as two antagonistic alleles that constitute an allorecognition system: the het-s allele encoding the protein variant capable of prion formation and the het-S allele encoding a protein variant that cannot form a prion. We document here that het-s alleles, capable of prion formation, are nearly twice as frequent as het-S alleles in a natural population of 112 individuals. Then, we report a 92% prevalence of [Het-s] prion infection among the het-s isolates and find evidence of the role of the [Het-s]/het-S allorecognition system on the incidence of infection by a deleterious senescence plasmid. We explain the het-s/het-S allele ratios by the existence of two selective forces operating at different levels. We propose that during the somatic stage, the role of [Het-s]/HET-S in allorecognition leads to frequency-dependent selection for which an equilibrated frequency would be optimal. However, in the sexual cycle, the [Hets] prion causes meiotic drive favoring the het-s allele. Our findings indicate that [Het-s] is a selected and, therefore, widespread prion whose activity as selfish genetic element is counteracted by balancing selection for allorecognition polymorphism.heterokaryon incompatibility | self/nonself recognition | spore killing

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