Divergence of the Yeast Transcription Factor FZF1 Affects Sulfite Resistance

Abstract

Changes in gene expression are commonly observed during evolution. However, the phenotypic consequences of expression divergence are frequently unknown and difficult to measure. Transcriptional regulators provide a mechanism by which phenotypic divergence can occur through multiple, coordinated changes in gene expression during development or in response to environmental changes. Yet, some changes in transcriptional regulators may be constrained by their pleiotropic effects on gene expression. Here, we use a genome-wide screen for promoters that are likely to have diverged in function and identify a yeast transcription factor, FZF1, that has evolved substantial differences in its ability to confer resistance to sulfites. Chimeric alleles from four Saccharomyces species show that divergence in FZF1 activity is due to changes in both its coding and upstream noncoding sequence. Between the two closest species, noncoding changes affect the expression of FZF1, whereas coding changes affect the expression of SSU1, a sulfite efflux pump activated by FZF1. Both coding and noncoding changes also affect the expression of many other genes. Our results show how divergence in the coding and promoter region of a transcription factor alters the response to an environmental stress.

A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum

“…3 and Supplementary Data 2). This gene has been shown to encode a fast-evolving transcription factor that regulates several genes, including the gene encoding Ssu1, an efflux pump involved in sulfite resistance 40 . All introgressions in this set also encompass the ZRT1 gene, which encodes a high affinity zinc transporter that was recently reported to exhibit a sequence signature of balancing selection in S. cerevisiae 41 .…”

Evolution of ecological dominance of yeast species in high‐sugar environments

“…Furthermore, sulfites are frequently added to wine must, and wine strains of S. cerevisiae are known to exhibit higher levels of sulfite resistance than nonwine strains (Pérez-Ortín et al 2002; Yuasa et al 2004). Interspecific differ-ences in sulfite resistance (Engle and Fay 2012), copper resistance (Warringer et al 2011), and other environmental conditions that we did not examine may thus contribute to S. cerevisiae's observed dominance of wine fermentations. Although we find S. paradoxus to be competitive with S. cerevisiae in controlled laboratory settings, it has been reported to be the dominant yeast species in only a few fermentations (Redzepović et al 2002;Valero et al 2007).…”

A new chromosomal rearrangement improves the adaptation of wine yeasts to sulfite

“…Strains lacking SSU1 gene are more sensitive to sulfite than their wild-type counterparts, because SSU1 deletion increases the accumulation of intracellular sulfite (Avram and Bakalinsky, 1997;Nadai et al, 2016). Another gene involved in yeast sulfite resistance is the transcription factor FZF1 (Casalone et al, 1992(Casalone et al, , 1994Avram et al, 1999;Engle and Fay, 2012). Fzf1 interacts with two regions of DNA (CS1 and CS2) immediately upstream of SSU1 and activates its transcription (Avram et al 1999;Saver et al, 2005).…”