Auxier, B. | Search bioRxiv

bioRxiv2021

Recombinant haplotypes reflect sexual reproduction in symbiotic arbuscular mycorrhizal fungi

Arbuscular mycorrhizal fungi (AMF) are part of the most widespread fungal-plant symbiosis. They colonize at least 80% of plant species, promote plant growth and plant diversity. These fungi are multinucleated and contain either one or two haploid nuclear genotypes (monokaryon and dikaryon) identified by the alleles at a putative mating-type locus. This taxon has been considered as an ancient asexual scandal because of the lack of observable sexual structures. Despite identification of a putative mating-type locus and functional activation of genes related to mating when two isolates co-exist, it remains unknown if AMF take part in a mainly sexual life cycle. We used publicly available genome sequences to test if dikaryon genomes display signatures of sexual reproduction in the form of reciprocal recombination patterns, or if they display signatures of parasexual reproduction involving gene conversion. We used short-read and long-read sequence data to identify nucleus genotype-specific haplotypes within dikaryons and then compared them to orthologous gene sequences from related monokaryon isolates displaying the same putative MAT-types. We observed that these genotype-specific haplotypes display reciprocal recombination and not gene conversion. These results are consistent with a sexual origin of the dikaryon rather than a parasexual origin and provides an important step to understand the life cycle of these globally important symbiotic fungi.

evolutionary biology↗

bioRxiv2020

Nuclear selection is effectively policed by mating restrictions of the dikaryotic life cycle of mushrooms.

Generally, sexual organisms contain two haploid genomes, one from each parent, united in a single diploid nucleus of the zygote which links their fate during growth. A fascinating exception to this are Basidiomycete fungi, where the two haploid genomes remain separate in a dikaryon, retaining the option to fertilize subsequent monokaryons encountered. How the ensuing nuclear competition influences the balance of selection within and between individuals is largely unexplored. We test the consequences of the dikaryotic lifecycle for mating success and mycelium-level fitness components. We assume a tradeoff between mating fitness at the level of the haploid nucleus and fitness of the fungal mycelium. We show that the maintenance of fertilization potential by dikaryons leads to a higher proportion of fertilized monokaryons, but that the ensuing intra-dikaryon selection for increased nuclear mating fitness leads to reduced mycelium fitness relative to a diploid life cycle. However, this fitness reduction is lower compared to a hypothetical life cycle where dikaryons can also exchange nuclei. Prohibition of fusion between dikaryons therefore reduces the level of nuclear parasitism. The number of loci influencing fitness is an important determinant of the degree to which average mycelium-level fitness is reduced. The results of this study crucially hinge upon a tradeoff between nucleus and mycelium-level fitness. We discuss the evidence for this assumption and the implications of an alternative that there is a positive relationship between nucleus and mycelium-level fitness.

evolutionary biology↗