Abstract
BackgroundFungi 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.ResultsThe 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.ConclusionsThe 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.
Highlights
Fungi are asexually and sexually reproducing organisms that can combine the evolutionary advantages of the two reproductive modes
In this study we aimed at elucidating the importance of sexual reproduction in the Phialocephala fortinii sensu lato - Acephala applanata species complex (PAC) that belongs to the dark septate endophytes, a polyphyletic group of ascomycetes with characteristic melanized, septate hyphae that commonly colonize roots of woody plant species [27]
In filamentous ascomycetes the mating type (MAT) locus is the key determinant of breeding system and it has been shown that conversions between heterothallism and homothallism can be achieved by manipulating the MAT locus [41,49]
Summary
Fungi are asexually and sexually reproducing organisms that can combine the evolutionary advantages of the two reproductive modes. 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. For many fungi, especially for filamentous ascomycetes, only part of their life cycle is known These taxa are classified as Deuteromycota or “fungi imperfecti” due to the lack of sexual morphology [13], but it is unclear whether sexual reproduction is absent, rare or cryptic because sexual morphology is often difficult to observe in nature or in the laboratory [14,15]. The importance of sexual reproduction in natural populations of such species remains an open question which can be addressed by direct and indirect approaches [16]
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