Full circle : Rise and fate of genetic variation in Marasmius oreades fairy rings

Sammanfattning: Genetic variation is a prerequisite for evolution. The degree of variability within a species is governed by forces including mutation, recombination and selection. In the kingdom of fungi, where periodic sexual reproduction may be interleaved with extended vegetative phases, generators of variability are not restricted to act only during sexual cycles. Such generators may be in the form of mutations to the genome, affecting single base pairs up to large-scale rearrangements, movement of transposable elements, or non-meiotic shuffling of genetic variants by mitotic recombination or parasexuality. Particularly in mushroom-forming fungi, where mycelia may become large and old, the evolutionary potential of variation acquired over vegetative growth is expected to be large. In this thesis, I have studied the rise and fate of variation gained during vegetative growth in the mushroom-forming fungus Marasmius oreades: a non-model species known for growing in ‘fairy rings’. By taking advantage of state-of-the-art genome sequencing technology and developing new bioinformatics methods, the genome sequence of M. oreades was successfully reconstructed. This resource was combined with genome re-sequencing to identify different types of mutations in M. oreades fairy rings, and to investigate the transmission of such mutations into the next generation through sexual spores. The results presented in this thesis reveal that the M. oreades genome is extremely stable at all levels during vegetative growth in its natural environment. Furthermore, the few mutations that arise do not seem to be transferred to the sexual spores. A significant amount of transposon movement was however revealed in monokaryotic strains when separated from dikaryons and grown in the laboratory. The combination of these results suggests that fungi possess an unknown system to suppress the accumulation of mutations during growth in nature, and that the apparent lack of a segregated germline in fungi potentially has to be reconsidered. Thus, contrary to expectations, the vegetative life stage in long-lived mushroom-forming fungi does not contribute much genetic variation, making these organisms more similar to animals and plants than previously considered. Further studies are needed to reveal how fungi control mutation accumulation, and elucidate if transposon activity is high also in naturally derived monokaryons in the form of meiotic progeny. The findings in this thesis add to what is known about how genetic variation is introduced into natural populations, how fungi deal with mutations, and highlight the complexity of genetic systems in mushroom-forming fungi.