Manifold anomalies in gene expression in a vineyard isolate of Saccharomyces cerevisiae revealed by DNA microarray analysis

Abstract

Genome-wide transcriptional profiling has important applications in evolutionary biology for assaying the extent of heterozygosity for alleles showing quantitative variation in gene expression in natural populations. We have used DNA microarray analysis to study the global pattern of transcription in a homothallic strain of Saccharomyces cerevisiae isolated from wine grapes in a Tuscan vineyard, along with the diploid progeny obtained after sporulation. The parental strain shows 2:2 segregation (heterozygosity) for three unlinked loci. One determines resistance to trifluoroleucine; another, resistance to copper sulfate; and the third is associated with a morphological phenotype observed as colonies with a ridged surface resembling a filigree. Global expression analysis of the progeny with the filigreed and smooth colony phenotypes revealed a greater than 2-fold difference in transcription for 378 genes (6% of the genome). A large number of the overexpressed genes function in pathways of amino acid biosynthesis (particularly methionine) and sulfur or nitrogen assimilation, whereas many of the underexpressed genes are amino acid permeases. These wholesale changes in amino acid metabolism segregate as a suite of traits resulting from a single gene or a small number of genes. We conclude that natural vineyard populations of S. cerevisiae can harbor alleles that cause massive alterations in the global patterns of gene expression. Hence, studies of expression variation in natural populations, without accompanying segregation analysis, may give a false picture of the number of segregating genes underlying the variation.

Heterologous expression of cellulase genes in natural Saccharomyces cerevisiae strains

“…Synergistic expression of cellulase genes for degradation of cellulosic substrates has been demonstrated by various studies (7,(99)(100)(101), and growth on cellulose has been accomplished through co-expression of cellulase genes in S. cerevisiae (102). Various hypotheses have been proposed to explain the mechanism of synergistic interactions, however research has shown that the extent of cellulase synergism is influenced by enzyme concentration and the nature of the lignocellulosic substrate (65), therefore synergism is dependent on the ratio of individual enzymes, the substrate saturation and the properties of the substrate (99).…”

The new mutation theory of phenotypic evolution

“…This can be explained partly by the presence of a high degree of protein polymorphism observed by electrophoresis at many loci (24,78). Recent studies have also shown that there is a large amount of variation in the level of gene expression among different alleles at a locus (79)(80)(81)(82)(83). In humans, it has been reported that, in 63% of the genes examined, the expression level of one allele is 2-fold or more greater than that of another allele (81).…”

Evaluating the role of natural selection in the evolution of gene regulation

“…Genome-wide measurements have revealed high rates of genetic variation in gene expression (typically 410% of genes) in humans (Enard et al, 2002;Rockman and Wray, 2002;Bray et al, 2003;Lo et al, 2003;Whitney et al, 2003;Morley et al, 2004;Pastinen et al, 2004;Radich et al, 2004), mice (Cowles et al, 2002;Schadt et al, 2003;Shockley and Churchill, 2006), fish (Oleksiak et al, 2002(Oleksiak et al, , 2005, flies (Jin et al, 2001;Wayne and McIntyre, 2002;Meiklejohn et al, 2003;Rifkin et al, 2003;Nuzhdin et al, 2004;Ranz et al, 2004), yeast (Cavalieri et al, 2000;Brem et al, 2002;Townsend et al, 2003;Yvert et al, 2003;Fay et al, 2004), plants (Kirst et al, 2005;Vuylsteke et al, 2005;Lai et al, 2006) and bacteria (Le et al, 2005). Patterns of expression divergence have also been compared between sexes (Jin et al, 2001;Ranz et al, 2003;Gibson et al, 2004), across developmental stages (Rifkin et al, 2003), among tissue types (Enard et al, 2002;Whitehead and Crawford, 2005;Khaitovich et al, 2005a, b) and over different environments (Fay et al, 2004;Landry et al, 2006).…”