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Unholy marriages and eternal triangles: how competition in the mushroom life cycle can lead to genomic conflict

Summary

Mushrooms reproduce in an unusual way where two separate genomes coexist peacefully in the same fungal body. However, this arrangement creates opportunities for selfish genetic elements to cheat and pursue their own interests at the expense of the whole organism. The authors explore how competition between these genetic components could drive evolution of new mating systems and characteristics in mushroom fungi.

Background

Mushroom-forming basidiomycetes have a unique sexual life cycle where gamete fusion is separated in time from genome mixing, and two haploid nuclei remain separate in dikaryotic cells. This unusual arrangement creates opportunities for genomic conflict that differ fundamentally from other sexual organisms like animals and plants.

Objective

To systematically explore the potential for genomic conflict in the basidiomycete life cycle resulting from competition among nuclei and between mitochondrial genomes. The authors identify sources of ultra-selfish genes that could be favored at the nuclear level but be deleterious to the organism as a whole.

Results

The analysis identifies two main categories of genomic conflict: mitochondrial-nuclear conflict due to different inheritance modes, and nuclear competition during vegetative growth and di-mon (Buller) matings. Mutations increasing nuclear competitive success could be selected even if they reduce overall dikaryon fitness, with maximum tolerable fitness reductions calculated at 25% for complete competitive dominance.

Conclusion

The basidiomycete life cycle, with separated nuclei in dikaryotic cells and hermaphroditic mating, creates unique opportunities for genomic conflict compared to diploid organisms. Evidence suggests life cycle transitions from outcrossing to selfing (as in Agaricus bisporus) and mating-type complexity may reflect this underlying genomic conflict.
  • Published in:Philosophical Transactions of the Royal Society B: Biological Sciences,
  • Study Type:Review,
  • Source: PMID: 27619697, DOI: 10.1098/rstb.2015.0533
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