Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts

Abstract

Understanding the evolutionary relationship between genome content and ecological niche is one of the fundamental challenges of biology. The distinct physiologies of yeast species provide a window into how genomes evolve in concert with niche. Although the enzymes of the well studied yeast galactose utilization pathway are present in all domains of life, we have found that multiple genes of the GAL pathway are absent from four yeast species that cannot use galactose. Whereas three species lack any trace of the pathway except a single gene, Saccharomyces kudriavzevii, a close relative of Saccharomyces cerevisiae, retains remnants of all seven dedicated GAL genes as syntenic pseudogenes, providing a rare glimpse of an entire pathway in the process of degeneration. An estimate of the timing of gene inactivation suggests that pathway degeneration began early in the lineage and proceeded rapidly. S. kudriavzevii exhibits several other divergent physiological properties that are associated with a shift in ecological niche. These results suggest that rapid and irreversible gene inactivation and pathway degeneration are associated with adaptation to new ecological niches in natural populations. Inactivated genes may generally serve as markers of specific functions made dispensable by recent adaptive shifts.

A de novo originated gene depresses budding yeast mating pathway and is repressed by the protein encoded by its antisense strand

“…Logically, if MDF1 was an old gene lost in other species, we would have to assume at least nine independent losses in 13 sequenced hemiascomycete lineages based on the phylogeny ( Figure 6A). This is in sharp contrast to the fact that most gene-loss events were confined to duplicated copies after whole genome duplications, which was after the split of the lineage leading to S. cerevisiae from K. lactis about 100 mya [24], and that the most extreme and rare multiple gene-loss cases only have independent gene losses in three or four lineages [25]. In addition, we reconstructed the ancestral consensus sequence of the region that corresponds to S. cerevisiae's MDF1 gene based on the sequences from the sensu stricto species, and found that there were at least two stop codons and two framesshifting indels in the common ancestor (Supplementary information, Figure S5), indicating that it is unlikely that the MDF1 gene was lost in all the other species but remained intact only in S. cerevisiae.…”

Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts

“…The passive loss of genes from genomes in which there is no selection to retain them is a familiar phenomenon in molecular evolution 20,21 . We suggest that passive gene loss is the likely mechanism of the original WGD event in yeast.…”

Evolution of gene network activity by tuning the strength of negative-feedback regulation

“…paradoxus is the closest relative of S. cerevisiae and the GAL network is an evolutionarily preserved network between the two species 6,10 . All four regulatory proteins (Gal2p, Gal3p, Gal4p and Gal80p) of the network have the same functional roles 10 in both species, and there are high levels of homology between the GAL network promoters and genes from both species.…”