Aneuploidy in yeast: Segregation error or adaptation mechanism?

Abstract

Aneuploidy is the loss or gain of chromosomes within a genome. It is often detrimental and has been associated with cell death and genetic disorders. However, aneuploidy can also be beneficial and provide a quick solution through changes in gene dosage when cells face environmental stress. Here, we review the prevalence of aneuploidy in Saccharomyces, Candida, and Cryptococcus yeasts (and their hybrid offspring) and analyse associations with chromosome size and specific stressors. We discuss how aneuploidy, a segregation error, may in fact provide a natural route for the diversification of microbes and enable important evolutionary innovations given the right ecological circumstances, such as the colonisation of new environments or the transition from commensal to pathogenic lifestyle. We also draw attention to a largely unstudied cross link between hybridisation and aneuploidy. Hybrid meiosis, involving two divergent genomes, can lead to drastically increased rates of aneuploidy in the offspring due to antirecombination and chromosomal missegregation. Because hybridisation and aneuploidy have both been shown to increase with environmental stress, we believe it important and timely to start exploring the evolutionary significance of their co-occurrence.

Keywords: adaptation; aneuploidy; environmental stress; hybridisation; yeast.

Figure 1

Diagram of the causes and consequences of aneuploidy. Sexual reproduction promoting aneuploidy includes hybridisation between divergent species followed by antirecombination during hybrid meiosis, and nondisjunction of sister chromatids in regular nonhybrid meiosis, leading to chromosomal missegregation. Aneuploidy can also occur due to nondisjunction during mitotic cell division and when strains are propagating under severe environmental stress. Solid arrows show known causal relationships; dashed arrows show hypothesized relationships

Figure 2

Aneuploidy as a temporary adaptation mechanism Redrawn from (Yona et al., 2012). When repeatedly subjected to high temperatures (yellow bolts), replicate diploid yeast populations (circles) gained an extra chromosome (red, blue, and green lines; only three of 16 chromosomes shown) within 450 generations of long‐term exposure to high temperatures. After 2,350 generations of exposure to high temperatures, euploidy was restored and novel beneficial mutations (indicated in yellow) compensated for the loss of the extra chromosome and increased fitness further

Figure 3

Proportion of aneuploid to euploid strains as a function of ploidy. Data was extracted from four sources (Duan et al., 2018; Gallone et al., 2016; Peter et al., 2018; Zhu et al., 2016) with a total of 1,547 strains between them (158 haploid, 1,149 diploid, 104 triploid, and 131 tetraploid). The proportion of aneuploid to euploid strains was calculated per study, means and standard errors were calculated across studies. Analyses and graphs were made in R version 3.5.1 (Feather Spray; R Core Team, 2018) with the packages ggplot2 (Wickham, 2016), ggpubr (Kassambara, 2018), and magrittr (Bache & Wickham, 2014). (Kruskal–Wallis χ ² = 9.86, p = .02, pairwise t‐test [4N] p < .05. ^* p < 0.05, ^** p < .01)

Figure 4

Number of aneuploidy incidents as a function of chromosome size. Data was extracted from eight sources (Duan et al., 2018; Gallone et al., 2016; Jaffe et al., 2017; Kao et al., 2010; Peter et al., 2018; Selmecki et al., 2015; Sharp et al., 2018; Zhu et al., 2016), with a total of 1,207 aneuploidies between them. Chromosomes are labelled with Roman numerals