Abstract

The basidiomycete Schizophyllum commune has the highest level of genetic polymorphism known among living organisms. In a previous study, it was also found to have a moderately high per-generation mutation rate of 2×10−8, likely contributing to its high polymorphism. However, this rate has been measured only in an experiment on Petri dishes, and it is unclear how it 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 rate of 1.24×10−7 substitutions per nucleotide per meter of growth, or ∼2.04×10−11 per nucleotide per cell division. In contrast to what has been observed in a number of species with extensive vegetative growth, this rate does not decline in the course of propagation of a mycelium. As a result, even a moderate per-cell-division mutation rate in S. commune can translate into a very high per-generation mutation rate when the number of cell divisions between consecutive meiosis is large.

Highlights

  • Mutation rate is the key parameter of evolution

  • We show that S. communeaccumulates 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 roburand the fungus Armillaria gallica

  • The per generation mutation rate in a multicellular organism is a product of the mutation rate per cell division and the number of mitoses between two consecutive meioses

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Summary

Introduction

Mutation rate is the key parameter of evolution. the development of next-generation sequencing technologies made it possible to measure mutations rates directly, and the data on different species are accumulating rapidly. Per nucleotide per generation mutation rate varies greatly between species, from ~10​-8​to ~10​-10-​10-​11,with multicellular eukaryotes tending to have higher rates (~10​-8-​10-​9)than unicellular organisms (~10​-9-​10-​11)(Lynch et al 2016). This is at least partially due to multiple cell divisions that occur in the course of a single generation in multicellular organisms. As long as germ line cell divisions keep occurring in the course of life of an individual, as in males of mammals, the number of mutations passed onto offspring increases with the age of reproduction, can produce a correlation between the age at reproduction (Kong et al 2012). Many species have a dedicated germline, in which the number of cell divisions is restricted; for example, the number of mutations passed to offspring by a human mother depends on her age only slightly (Jónsson et al 2017), probably because maternal germline does not divide for most of her life

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