Stage-specific transposon activity in the life cycle of the fairy-ring mushroom Marasmius oreades

Abstract

Genetic variability can be generated by different mechanisms, and across the life cycle. Many basidiomycete fungi have an extended somatic stage, during which each cell carries two genetically distinct haploid nuclei (dikaryosis), resulting from fusion of two compatible monokaryotic individuals. Recent findings have revealed remarkable genome stability at the nucleotide level during dikaryotic growth in these organisms, but whether this pattern extends to mutations affecting large genomic regions remains unknown. Furthermore, despite high genome integrity during dikaryosis, basidiomycete populations are not devoid of genetic diversity, begging the question of when this diversity is introduced. Here, we used a Marasmius oreades fairy ring to investigate the rise of large-scale variants during mono- and dikaryosis. By separating the two nuclear genotypes from four fruiting bodies and generating complete genome assemblies, we gained access to investigate genomic changes of any size. We found that during dikaryotic growth in nature the genome stayed intact, but after separating the nucleotypes into monokaryons, a considerable amount of structural variation started to accumulate, driven to large extent by transposons. Transposon insertions were also found in monokaryotic single-meiospore isolates. Hence, we show that genome integrity in basidiomycetes can be interrupted during monokaryosis, leading to genomic rearrangements and increased activity of transposable elements. We suggest that genetic diversification is disproportionate between life cycle stages in mushroom-forming fungi, so that the short-lived monokaryotic growth stage is more prone to genetic changes than the dikaryotic stage.

Extreme overall mushroom genome expansion in Mycena s.s. irrespective of plant hosts or substrate specializations

“…Recent research has found that fungi are much more prone to mutations and TE proliferations in the monokaryotic rather than the dikaryotic stage. 92 A non-adaptive reason for the extreme Arctic genome sizes (and TE proliferations) might thus be that Arctic mushrooms simply experience a much longer fraction of their lifetime as monokaryons waiting for a compatible partner to land, compared to temperate mushrooms with larger population sizes. Both adaptive and non-adaptive Arctic effects on Mycena specifically and mushrooms more generally should be tested more directly in future research on Arctic mushroom genomes compared to close non-Arctic relatives.…”

Runs of homozygosity reveal contrasting histories of inbreeding across global lineages of the edible porcini mushroom, Boletus edulis

“…The resulting loss of heterozygosity (LOH) could potentially be conflated with ROHs. However, LOHs are generated through mitotic recombination in diploid (more often in polyploid) nuclei (Dutta et al., 2022), a process that should be less common in Basidiomycete species that predominantly persist as dikaryons such as B. edulis , since both haploid nuclei go through mitosis separately (Hiltunen et al., 2022). Therefore, we believe the ROHs we detected in our study are true signals of genomic inbreeding, which is supported by the observation that geographical and ecological variables explain a significant amount of the variation in F ROH .…”

Reproducible evaluation of transposable element detectors with McClintock 2 guides accurate inference of Ty insertion patterns in yeast

“…The original McClintock system automated installation of these six “component” TE detection methods, provided a common interface to run all components, reduced the number of shared input files, and generated a standard set of output files [15]. Since its initial development, the McClintock system has been used to support detection of TE insertions and enable biological discoveries in a variety of organisms and biological contexts [15, 16, 17, 18, 19, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44] and to facilitate comparative evaluation of multiple TE detectors [15, 16, 45].…”