A little bit of sex prevents mutation accumulation even in apomictic polyploid plants

Ladislav Hodač,Timothy F Sharbel,Diego Hojsgaard,Simone Klatt,Elvira Hörandl

doi:10.1186/s12862-019-1495-z

Abstract

BackgroundIn the absence of sex and recombination, genomes are expected to accumulate deleterious mutations via an irreversible process known as Muller’s ratchet, especially in the case of polyploidy. In contrast, no genome-wide mutation accumulation was detected in a transcriptome of facultative apomictic, hexaploid plants of the Ranunculus auricomus complex. We hypothesize that mutations cannot accumulate in flowering plants with facultative sexuality because sexual and asexual development concurrently occurs within the same generation. We assume a strong effect of purging selection on reduced gametophytes in the sexual developmental pathway because previously masked recessive deleterious mutations would be exposed to selection.ResultsWe test this hypothesis by modeling mutation elimination using apomictic hexaploid plants of the R. auricomus complex. To estimate mean recombination rates, the mean number of recombinants per generation was calculated by genotyping three F1 progeny arrays with six microsatellite markers and character incompatibility analyses. We estimated the strength of purging selection in gametophytes by calculating abortion rates of sexual versus apomictic development at the female gametophyte, seed and offspring stage. Accordingly, we applied three selection coefficients by considering effects of purging selection against mutations on (1) male and female gametophytes in the sexual pathway (additive, s = 1.000), (2) female gametophytes only (s = 0.520), and (3) on adult plants only (sporophytes, s = 0.212). We implemented recombination rates into a mathematical model considering the three different selection coefficients, and a genomic mutation rate calculated from genome size of our plants and plant-specific mutation rates. We revealed a mean of 6.05% recombinants per generation. This recombination rate eliminates mutations after 138, 204 or 246 generations, depending on the respective selection coefficients (s = 1.000, 0.520, and 0.212).ConclusionsOur results confirm that the empirically observed frequencies of facultative recombination suffice to prevent accumulation of deleterious mutations via Muller’s ratchet even in a polyploid genome. The efficiency of selection is in flowering plants strongly increased by acting on the haplontic (reduced) gametophyte stage.

Highlights

In the absence of sex and recombination, genomes are expected to accumulate deleterious mutations via an irreversible process known as Muller’s ratchet, especially in the case of polyploidy
Pairwise genetic distances between genotypes showed that most progenies were clonal and identical to the respective mother genotype, but non-maternal offspring appeared in all three progenies
A facultative asexual plant population with a non-zero recombination rate per generation and with one fixed deleterious mutation consists of three different offspring classes in the first generation (Additional file 3a)

Summary

Introduction

In the absence of sex and recombination, genomes are expected to accumulate deleterious mutations via an irreversible process known as Muller’s ratchet, especially in the case of polyploidy. We assume a strong effect of purging selection on reduced gametophytes in the sexual developmental pathway because previously masked recessive deleterious mutations would be exposed to selection. A novel hypothesis by [11] for flowering plants predicted that even in high polyploids, low rates of facultative sexuality would suffice to counteract mutation accumulation This model is based on the consideration of three features specific for flowering plants: First, a sporophyte generation (the familiar green plant) and a gametophyte generation (embryo sac and pollen) alternate during the life cycle, which can increase the efficacy of haploid selection [12]. Plants reproducing via apomixis (i.e., clonal reproduction via seed), develop a female gametophyte from an initial cell that has not undergone meiosis These egg cells are unreduced, nonrecombinant, and develop parthenogenetically into embryos. Though polyploids would supposedly have an increased absolute number of mutations because of a higher number of possible mutation sites, recessive mutations would not become expressed in the heterozygous state [9, 12]

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