Modeling the Consequences of the Dikaryotic Life Cycle of Mushroom-Forming Fungi on Genomic Conflict

Summary

This research uses computer modeling to understand how mushroom-forming fungi maintain an unusual reproductive strategy where two separate nuclei coexist in each cell. The study reveals important trade-offs between reproductive success and overall fitness of the fungus. This has implications for understanding fungal evolution and reproduction. Impacts on everyday life: – Helps explain how mushrooms and other fungi reproduce and evolve – Provides insights into managing fungal crops and preventing fungal diseases – Advances our understanding of trade-offs in biological systems – Could inform strategies for breeding improved mushroom varieties – Demonstrates how computer models can help understand complex biological processes

Background

Sexual organisms typically contain two haploid genomes united in a single diploid nucleus after fertilization. Basidiomycete fungi are unique in that the two haploid genomes remain separate in a dikaryon state, retaining the ability to fertilize additional monokaryons. This creates potential for nuclear competition and genomic conflict, but the evolutionary consequences are not well understood.

Objective

To test the consequences of the dikaryotic life cycle for mating success and mycelium-level fitness components, assuming a trade-off between nuclear mating fitness and fungal mycelium fitness. The study aimed to model and compare three scenarios: diploid life cycle, standard dikaryon with di-mon mating, and hypothetical open dikaryon with unrestricted nuclear exchange.

Results

The maintenance of fertilization potential by dikaryons led to a higher proportion of fertilized monokaryons, but intradikaryon selection for increased nuclear mating fitness resulted in reduced mycelium fitness compared to a diploid life cycle. The fitness reduction was lower in standard dikaryons versus hypothetical open dikaryons. The number of fitness-related loci was an important determinant of mycelium-level fitness reduction. Restriction of nuclear exchange between dikaryons reduced nuclear parasitism.

Conclusion

The dikaryotic life cycle creates inherent tension between selection at nuclear and mycelial levels. While allowing increased mating opportunities, it can lead to reduced mycelial fitness due to nuclear competition. The costs are minimized by restricting nuclear exchange to di-mon matings and when fitness variance is limited to a single locus. The persistence of the dikaryotic state over 400 million years suggests mechanisms must exist to police nuclear competition.
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