Evolutionary significance of imbalanced nuclear ratios within heterokaryons of the basidiomycete fungus Heterobasidion parviporum

Many fungi have heterokaryotic life stages in which genetically different nuclei inhabit the same cell. In basidiomycetes, the heterokaryon is the product of mating and represents a genomic union very similar to a diploid thallus, yet the maintenance of unfused nuclei suggests a more complex association of the two genomes relative to diploidy. In species with variable numbers of nuclei per heterokaryotic cell, nuclear ratios within a mycelium may possibly become imbalanced (differ from 1:1) due to nuclear competition. In this study, heterokaryons of the basidiomycete Heterobasidion parviporum were examined to determine the effects of genotype and environment on nuclear ratios within vegetative mycelia. The data reveal that nuclear ratios are frequently imbalanced, generally stable over time, and genetically determined. The nuclear ratios were affected by environment, but the observed nuclear ratios did not follow the expectations of strong selection acting on a population of nuclei. Instead, these ratios were largely driven by genetic effects and epigenetic effects. Finally, the data suggest that nuclear ratio imbalance also affects both gene transcription and growth rate, implying that heterokaryotic basidiomycetes are not functionally equivalent to diploid individuals and have a higher potential for genotypic and phenotypic variation.