Rapid Expansion and Functional Divergence of Subtelomeric Gene Families in Yeasts

Abstract

Summary Background Subtelomeres, regions proximal to telomeres, exhibit characteristics unique to eukaryotic genomes. Genes residing in these loci are subject to epigenetic regulation and elevated rates of both meiotic and mitotic recombination. However, most genome sequences do not contain assembled subtelomeric sequences, and, as a result, subtelomeres are often overlooked in comparative genomics. Results We study the evolution and functional divergence of subtelomeric gene families in the yeast lineage. Our computational results show that subtelomeric families are evolving and expanding much faster than families that do not contain subtelomeric genes. Focusing on three related subtelomeric MAL gene families involved in disaccharide metabolism that show typical patterns of rapid expansion and evolution, we show experimentally how frequent duplication events followed by functional divergence yields novel alleles that allow metabolism of different carbohydrates. Conclusions Taken together, our computational and experimental analyses show that the extraordinary instability of eukaryotic subtelomeres supports rapid adaptation to novel niches by promoting gene recombination and duplication followed by functional divergence of the alleles.

Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast

“…2 A and B). The transferred fragment carries the S. cerevisiae IMA1 (YGR287C) gene that encodes isomaltase, which catalyzes cleavage of the disaccharide isomaltose (32). The identical breakpoints indicate a common origin for this S. cerevisiae sugar-processing gene in all three hybrid strains and suggest strong selection for optimal sugar utilization during brewing.…”

Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments

“…Since it is likely that many of the non-S288c genomic sequences are located subtelomerically (Novo et al 2009)-and this is also intimated by the fact that our clusters from subtelomeric regions were similar to those generated from non-S288c sequences-we interpret our data as showing that most of the copy number variation observed among these 83 diverse S. cerevisiae industrial strains occurred either in the subtelomeric regions or among the classes of transposable elements. This has been noted before (e.g., Dunn et al 2005;Brown et al 2010); however, in this study we have generated the most comprehensive catalog of copy number variation among a wide variety of Saccharomyces strains thus far.…”

“…Subtelomeric gene families evolve faster than their internal counterparts, and subtelomeric regions are more frequently the sites of gene duplication (Ames et al 2010), suggesting a ''unique role of subtelomeres as hotbeds for genomic evolution and innovation'' (Brown et al 2010). For example, a presumed adaptive amplification of the subtelomeric SNO/SNZ genes has been shown to occur in fuel ethanol strains (Stambuk et al 2009), and the subtelomeric location of sugar utilization genes has long been assumed to be adaptive (e.g., Brown et al 2010). In addition, several transposable element families show variation in presence or absence, as well as copy number, in different strains, accounting for a large amount of genome diversity among the Saccharomyces yeasts .…”

Saccharomyces cerevisiae Forms d-2-Hydroxyglutarate and Couples Its Degradation to d-Lactate Formation via a Cytosolic Transhydrogenase

“…The latter is localized in the subtelomeric region (at 16 kb from the telomere) of the left arm of chromosome V in S. cerevisiae. Genes in subtelomeric regions are evolving faster than the rest of the genome (41) leading to frequent duplication or gene loss events, notably in the case of large gene families such as the PAU, HXT, or MAL gene families (42)(43)(44). To quantify the selective pressure on the DLD3 gene, we compared the rate of substitutions at non-synonymous sites (dN) and at synonymous sites (dS) based on pairwise alignments of nucleic acid sequences from 40 S. cerevisiae species.…”