Biology subjects

Aanen, D. K.

Publications and source records attributed to Aanen, D. K..

6 recordsLinked to original sources

bioRxiv2026

Genetic Association of Somatic Incompatibility and NLR-like Protein Domains in Coprinopsis cinerea

In fungi, hyphal fusion is beneficial within an individual, but fusion between individuals comes with the risks of infection or exploitation. To manage this risk, fungi have developed mechanisms to restrict sustained fusion to be within a genetic individual, called allorecognition. In Ascomycete fungi, this recognition is based on allelic identity at several polymorphic allorecognition genes, often triggering cell death. However, the genetic basis of allorecognition is unknown in basidiomycetes, the clade that includes mushroom-forming fungi. Here, we map the first locus for this trait, which we call somA, in the mushroom-forming fungus Coprinopsis cinerea. We combined F1 offspring phenotypes with independent backcross lines to identify a region on chromosome 5 linked with the production of a barrage zone, a classic allorecognition phenotype. Fine-mapping of this region resulted in a region with a set of kinases and NACHT domain proteins, flanked by a leucine-rich repeat (LRR) protein. While the NACHT and kinase proteins are diverse between the parents, the LRR-encoding protein shows signs of purifying selection. Additional C. cinerea genomes show that this region contains several highly divergent alleles, consistent with long-term balancing selection. These polymorphic alleles all contain a single monomorphic LRR, which may indicate a novel mechanism for fungal nonself recognition. Based on a phylogenetic survey of related Basidiomycetes, this specific locus architecture appears to be restricted to closely related species. This finding of a multiallelic locus may explain the general trend of few nonself recognition loci in basidiomycetes. These results provide a first understanding of how individuality is maintained in basidiomycetes. Significance StatementHow mushroom-forming fungi recognize each other as individuals is an open question. Here, we identify the first genes that trigger this recognition in a mushroom-forming fungus. As these fungi have very distinctive lifecycles compared to mold-forming fungi, it was hypothesized that the process would operate from different mechanisms. Our results show the molecular mechanisms are in fact quite similar. These results provide a first step towards understanding how these fungi can both fuse with themselves and still discriminate against other individuals.

genetics↗

bioRxiv2025

Genetic mapping and nuclear interactions of an incompatibility response in Agaricus bisporus

During cultivation, mixing of different heterokaryotic individuals of the button mushroom, Agaricus bisporus, generally reduces yield. This phenomenon could be caused by direct antagonistic responses and/or reduced synchronization by not forming a chimeric hyphal network. In other fungi, highly divergent alleles for a set of genes affect successful network formation between individuals either by preventing fusion or, more commonly, triggering cell death post-fusion. To understand this process in A. bisporus, it is important to identify the allelic variants allowing these fungi to discriminate self from nonself. We leverage a recently described cell death staining method utilizing Evans Blue to visualize mycelial compatibility. Here, we provide results of a first genetic mapping of incompatibility alleles in A. bisporus. Crossing strains between A. bisporus var. bisporus and A. bisporus var. burnetti we find segregation ratios of compatible progeny generally consistent with three nuclear loci. To identify these regions, we first use a set of single Chromosome Substitution Lines (CSLs), produced by genotyping progeny with recombination skewed to the very chromosome ends. We localize the main effect to be between two and three chromosomes, depending on the common nucleus of interacting heterokaryons. Using genome-wide markers for 167 sexual progeny, we identify loci controlling mycelial compatibility on chromosomes 4, 6 and 7, the same chromosomes as indicated by chromosome substitution lines. Notably, while the choice of a common nucleus seemed to affect the compatibility of CSLs, it did not seem to affect the loci identified in the sexual progeny. The ability to mix different strains of this mushroom-forming fungus could allow additional cultivation approaches, combining strains with complementary characteristics. These results provide a starting point towards understanding the molecular mechanisms underlying this fundamental property of hyphal networks in basidiomycetes.

genetics↗

bioRxiv2022

Identification of heterokaryon incompatibility genes in Aspergillus fumigatus highlights a narrow footprint of ancient balancing selection

In fungi, a phenomenon termed heterokaryon incompatibility restricts hyphal fusion to occur within an individual since fusion between individuals leads to cell death. Generally, the genes involved are found to be under balancing selection from negative frequency dependent fitness. Here, we assess this in Aspergillus fumigatus, a human pathogenic fungus with an extremely high crossover rate. Using auxotrophic markers we screened sexual progeny for compatibility to identify genes involved in this process, the so-called het genes. In total, 5/148 (3.4%) offspring were compatible with a parent and 166/2142 (7.7%) sibling pairs were compatible, consistent with several segregating incompatibility loci. Genetic mapping resulted in five loci, four of which could be fine mapped to individual genes, of which we tested three through heterologous expression, confirming their causal relationship. Surprisingly, a population-level analysis of two available independent datasets did not show an increase in Tajimas D near these loci, normally a hallmark of balancing selection. However, analysis of closely related species did show trans-species polymorphisms across >10 million years, and equal allele frequencies within A. fumigatus. Using available de novo assemblies, we show that these balanced polymorphisms are restricted to within several hundred base pairs flanking the coding sequence, potentially due to this species high crossover rate. In addition to identifying the first het genes in an Aspergillus species, this work highlights the interaction of long-term balancing selection with a high recombination rate. Future mechanistic work on these het genes may provide novel routes for clinical therapies, as well as opportunities for strain improvement in biotechnology.

evolutionary biology↗

bioRxiv2020

Somatic deficiency causes reproductive parasitism in a fungus

Some multicellular organisms can fuse because mergers potentially provide mutual benefits. However, experimental evolution in the fungus Neurospora crassa has demonstrated that free fusion of mycelia favours cheater lineages, but the mechanism and evolutionary dynamics of dishonest exploitation are unknown. Here we show, paradoxically, that all convergently evolved cheater lineages have similar fusion deficiencies. These mutants are unable to initiate fusion but retain access to wild-type mycelia that fuse with them. This asymmetry reduces cheater-mutant contributions to somatic substrate-bound hyphal networks, but increases representation of their nuclei in the aerial reproductive hyphae. Cheaters only benefit when relatively rare and likely impose genetic load reminiscent of germline senescence. We show that the consequences of somatic fusion can be unequally distributed among fusion partners, with the passive non-fusing partner profiting more. We discuss how our findings may relate to the extensive variation in fusion frequency of fungi found in nature.

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↗

bioRxiv2018

Nuclear arms races: experimental evolution for mating success in the mushroom-forming fungus Schizophyllum commune

When many gametes compete to fertilize a limited number of compatible gametes, sexual selection will favour traits that increase competitive success during mating. In animals and plants, sperm and pollen competition have yielded many interesting adaptations for improved mating success. In fungi, similar processes have not been shown directly yet. We test the hypothesis that sexual selection can increase competitive fitness during mating, using experimental evolution in the mushroom-forming fungus Schizophyllum commune (Basidiomycota). Mating in mushroom fungi occurs by donation of nuclei to a mycelium. These fertilizing male nuclei migrate through the receiving female mycelium. In our setup, an evolving population of nuclei was serially mated with a non-evolving female mycelium for 20 sexual generations. From the twelve tested evolved lines, four had increased and one had decreased fitness relative to an unevolved competitor. Even though only two of those five remained significant after correcting for multiple comparisons, for all five lines we found a correlation between the efficiency with which the female mycelium is accessed and fitness, providing additional circumstantial evidence for fitness change in those five lines. In two lines, fitness change was also accompanied by increased spore production. The one line with net reduced competitive fitness had increased spore production, but reduced fertilisation efficiency. We did not find trade-offs between male reproductive success and other fitness components. We compare these findings with examples of sperm and pollen competition and show that many similarities between these systems and nuclear competition in mushrooms exist.

evolutionary biology↗