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.

The rate of whole-genome duplication can be accelerated by hybridization

“…S11, S12). Chromosome loss, consistent with previous studies (for review 44 ), more frequently affects the smallest chromosomes (I and III) in diploid hybrids, probably because it affects a smaller number of genes. However, larger chromosome losses (II, V and VIII) are observed in tetraploids, suggesting a potentially less deleterious effect of their loss due to the multiple copies present in the cell.…”

Heat Shock Drives Genomic Instability and Phenotypic Variations in Yeast

“…Aneuploidy, large-scale chromosomal rearrangements, and LOH are ubiquitous genomic alterations in solid tumor cells, as well as in yeast population (Zhu et al 2016, Heil et al 2017, Sansregret and Swanton 2017, Cho and Jinks-Robertson 2019, Gilchrist and Stelkens 2019. Many studies suggest that these genetic events would promote the adaptive evolution of yeast cells in response to environmental stimulus or genetic perturbations (Tan et al 2013, Gerstein et al 2015, Heil et al 2017, Hose et al 2015.…”

A Saccharomyces paradox: chromosomes from different species are incompatible because of anti-recombination, not because of differences in number or arrangement

“…Then, when the environment changes back or when other adaptive mutations optimising the specific trait under selection relieve the stress, the ancestral configuration could be restored, readying the population for the next unpredictable change. Indeed, authors have suggested that this kind of reversible chromosomal change in yeast might itself be a general adaptive strategy to an unpredictably changing environment (Gilchrist and Stelkens 2019, Dunham et al 2002, Infante et al 2003, Cox and Bevan 1962. If this inference is correct, we would predict that the rate of production of chromosomal variants would evolve to reflect the probability of environmental fluctuation, as a form of biological bet-hedging (de Jong et al 2011).…”