A stepwise route to polyploidy in yeast

Abstract

Polyploidy, the presence of multiple chromosome sets within a genome, is widespread and has played a major role in genome evolution in plants, fungi, and animals. Although polyploidization is generally attributed to mitotic genome doubling or unreduced gamete fusion, the mechanisms underlying ploidy increases, particularly triploid formation, remain unclear. Here, we identify a novel route to autopolyploidization in Saccharomyces cerevisiae, termed Sporulate-Endoreplicate-Mate (SEM), in which one gamete, or spore, undergoes postmeiotic endoreplication and subsequently mates with a nearby non-endoreplicated sibling spore after ascus breakdown, increasing ploidy by one haploid genome. We experimentally demonstrate stepwise transitions from diploidy to triploidy and from triploidy to tetraploidy. Intact asci can spontaneously generate new triploid and tetraploid strains upon one or two successive SEM cycles. Natural polyploids exhibit genomic signatures consistent with SEM being a major natural route to polyploidization in yeast. SEM establishes triploids as central intermediates in yeast polyploidization, analogous to the triploid bridge described in plants, and raises the possibility that a similar mechanism may contribute to polyploid genome formation in other eukaryotes.