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Background  Fungi are asexually and sexually reproducing organisms that can combine the evolutionary advantages of the two reproductive modes. However, for many fungi the sexual cycle has never been observed in the field or  in vitro  and it remains unclear whether sexual reproduction is absent or cryptic. Nevertheless, there are indirect approaches to assess the occurrence of sex in a species, such as population studies, expression analysis of genes involved in mating processes and analysis of their selective constraints. The members of the  Phialocephala fortinii  s. l. -  Acephala applanata  species complex (PAC) are ascomycetes and the predominant dark septate endophytes that colonize woody plant roots. Despite their abundance in many ecosystems of the northern hemisphere, no sexual state has been identified to date and little is known about their reproductive biology, and how it shaped their evolutionary history and contributes to their ecological role in forest ecosystems. We therefore aimed at assessing the importance of sexual reproduction by indirect approaches that included molecular analyses of the mating type ( MAT ) genes involved in reproductive processes.    Results  The study included 19 PAC species and > 3, 000 strains that represented populations from different hosts, continents and ecosystems. Whereas  A. applanata  had a homothallic (self-fertile)  MAT  locus structure, all other species were structurally heterothallic (self-sterile). Compatible mating types were observed to co-occur more frequently than expected by chance. Moreover, in > 80% of the populations a 1:1 mating type ratio and gametic equilibrium were found.  MAT  genes were shown to evolve under strong purifying selection.    Conclusions  The signature of sex was found in worldwide populations of PAC species and functionality of  MAT  genes is likely preserved by purifying selection. We hypothesize that cryptic sex regularely occurs in the PAC and that further field studies and  in vitro  crosses will lead to the discovery of the sexual state. Although structurally heterothallic species prevail, it cannot be excluded that homothallism represents the ancestral breeding system in the PAC.

Sex in the PAC: A hidden affair in dark septate endophytes?