Ancient evolutionary trade-offs between yeast ploidy states

PLoS Genet. 2013 Mar;9(3):e1003388. doi: 10.1371/journal.pgen.1003388. Epub 2013 Mar 21.

Abstract

The number of chromosome sets contained within the nucleus of eukaryotic organisms is a fundamental yet evolutionarily poorly characterized genetic variable of life. Here, we mapped the impact of ploidy on the mitotic fitness of baker's yeast and its never domesticated relative Saccharomyces paradoxus across wide swaths of their natural genotypic and phenotypic space. Surprisingly, environment-specific influences of ploidy on reproduction were found to be the rule rather than the exception. These ploidy-environment interactions were well conserved across the 2 billion generations separating the two species, suggesting that they are the products of strong selection. Previous hypotheses of generalizable advantages of haploidy or diploidy in ecological contexts imposing nutrient restriction, toxin exposure, and elevated mutational loads were rejected in favor of more fine-grained models of the interplay between ecology and ploidy. On a molecular level, cell size and mating type locus composition had equal, but limited, explanatory power, each explaining 12.5%-17% of ploidy-environment interactions. The mechanism of the cell size-based superior reproductive efficiency of haploids during Li(+) exposure was traced to the Li(+) exporter ENA. Removal of the Ena transporters, forcing dependence on the Nha1 extrusion system, completely altered the effects of ploidy on Li(+) tolerance and evoked a strong diploid superiority, demonstrating how genetic variation at a single locus can completely reverse the relative merits of haploidy and diploidy. Taken together, our findings unmasked a dynamic interplay between ploidy and ecology that was of unpredicted evolutionary importance and had multiple molecular roots.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biological Evolution
  • Cell Size / drug effects
  • Chromosomes / drug effects
  • Chromosomes / genetics
  • Copper / toxicity
  • Diploidy*
  • Ecology
  • Evolution, Molecular*
  • Gene-Environment Interaction
  • Genes, Mating Type, Fungal / drug effects
  • Genes, Mating Type, Fungal / genetics
  • Genotype
  • Haploidy*
  • Lithium / toxicity
  • Reproduction / drug effects
  • Reproduction / genetics
  • Saccharomyces cerevisiae / genetics*

Substances

  • Copper
  • Lithium

Grant support

This work was supported by the Royal Swedish Academy of Science to JW (http://www.kva.se/en/), the Swedish Cancer Society http://www.cancerfonden.se/ (10-0633) to PS, Carl Trygger's Foundation (http://www.carltryggersstiftelse.se/) to PS (11:454) and JW (08-400), and the European Commission UNICELLSYS programme (http://www.unicellsys.eu/) (LSHG-CT2007-201142) to PS and AB. EG was the recipient of a FEBS post-doctoral fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.