Additions, Losses, and Rearrangements on the Evolutionary Route from a Reconstructed Ancestor to the Modern Saccharomyces cerevisiae Genome

Open Access
Publisher Website
Google Scholar
Abstract
Comparative genomics can be used to infer the history of genomic rearrangements that occurred during the evolution of a species. We used the principle of parsimony, applied to aligned synteny blocks from 11 yeast species, to infer the gene content and gene order that existed in the genome of an extinct ancestral yeast about 100 Mya, immediately before it underwent whole-genome duplication (WGD). The reconstructed ancestral genome contains 4,703 ordered loci on eight chromosomes. The reconstruction is complete except for the subtelomeric regions. We then inferred the series of rearrangement steps that led from this ancestor to the current Saccharomyces cerevisiae genome; relative to the ancestral genome we observe 73 inversions, 66 reciprocal translocations, and five translocations involving telomeres. Some fragile chromosomal sites were reused as evolutionary breakpoints multiple times. We identified 124 genes that have been gained by S. cerevisiae in the time since the WGD, including one that is derived from a hAT family transposon, and 88 ancestral loci at which S. cerevisiae did not retain either of the gene copies that were formed by WGD. Sites of gene gain and evolutionary breakpoints both tend to be associated with tRNA genes and, to a lesser extent, with origins of replication. Many of the gained genes in S. cerevisiae have functions associated with ethanol production, growth in hypoxic environments, or the uptake of alternative nutrient sources. Genomes evolve in structure as well as in DNA sequence. We used data from 11 different yeast species to investigate the process of structural evolution of the genome on the evolutionary path leading to the bakers' yeast S. cerevisiae. We focused on an ancestor that existed about 100 million years ago. We were able to deduce almost the complete set of genes that existed in this ancestor and the order of these genes along its chromosomes. We then identified the complete set of more than 100 structural rearrangements that occurred as this ancestor evolved into S. cerevisiae and found that some places in the genome seem to be fragile sites that have been broken repeatedly during evolution. We also identified 124 genes that must be relatively recent additions into the S. cerevisiae genome because they were not present in this ancestor. These genes include several that play roles in the unique lifestyle of this species, as regards the intensive production and consumption of alcohol.