Rapid accumulation of mutations in growing mycelia of a hypervariable fungus Schizophyllum commune

Abstract

The number of mutations that occur per nucleotide per generation varies between species by several orders of magnitude. In multicellular eukaryotes, the per generation mutation rate depends both on the per cell division mutation rate and on the number of germline cell divisions per generation. In a range of species, from fungi to humans, the number of germline cell divisions is lower than that of somatic cells, reducing the mutation burden on the offspring. The basidiomycete Schizophyllum commune has the highest level of genetic polymorphism known among eukaryotes. In a previous study, it was also found to have a high per generation mutation rate, probably contributing to its high polymorphism. However, this rate has been measured only in a breeding experiment on Petri dishes, and it is unclear how this result translates to natural populations. Here, we used an experimental design that measures the rate of accumulation of de novo mutations in a linearly growing mycelium. We show that S. commune accumulates mutations at a uniform rate of 1.4·10−7 substitutions per nucleotide per meter of growth, which is 3 orders of magnitude higher than the corresponding rates in the oak Quercus robur and the fungus Armillaria gallica. This figure is consistent with the estimate obtained before, and suggests the lack of a dedicated germline in this system. If so, even a low per cell division mutation rate can translate into a very high per generation mutation rate when the number of cell divisions between consecutive meioses is large.