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Transcriptional rewiring of fungal galactose-metabolism circuitry.

ABSTRACT: The Leloir-pathway genes encode the enzymatic machinery involved in the metabolism of galactose.In the distantly related fungi Saccharomyces cerevisiae and Candida albicans, the genes encoding these enzymes are syntenically arranged, but the upstream regulatory regions are highly divergent. In S. cerevisiae, the Leloir-pathway genes are positively regulated by Gal4p acting through the UAS(G) sequence CGG(N(11))CCG. However, in C. albicans, the Gal4p and UAS(G) combination is found to regulate genes unrelated to galactose metabolism. We identified a palindromic sequence that acts to control GAL10 expression in C. albicans in the presence of galactose. This palindrome is found upstream of other Leloir-pathway genes in C. albicans, and in the absence of other regulatory sequences, activation of expression through this sequence in the presence of galactose requires Cph1p, the homolog of the Ste12p transcription factor of S. cerevisiae.Although the cellular process of galactose induction of the Leloir pathway is conserved between the two organisms, the regulatory circuits achieving the cellular process are completely distinct.

SUBMITTER: Martchenko M

PROVIDER: S-EPMC3842258 | biostudies-literature | 2007 Jun

REPOSITORIES: biostudies-literature

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Transcriptional rewiring of fungal galactose-metabolism circuitry.

Martchenko Mikhail M Levitin Anastasia A Hogues Herve H Nantel Andre A Whiteway Malcolm M

Current biology : CB 20070531 12

<h4>Background</h4>The Leloir-pathway genes encode the enzymatic machinery involved in the metabolism of galactose.<h4>Results</h4>In the distantly related fungi Saccharomyces cerevisiae and Candida albicans, the genes encoding these enzymes are syntenically arranged, but the upstream regulatory regions are highly divergent. In S. cerevisiae, the Leloir-pathway genes are positively regulated by Gal4p acting through the UAS(G) sequence CGG(N(11))CCG. However, in C. albicans, the Gal4p and UAS(G) ...[more]

PMID: 17540568

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Project description:Ethanol is the main by-product of yeast sugar fermentation that affects microbial growth parameters, being considered a dual molecule, a nutrient and a stressor. Previous works demonstrated that the budding yeast arose after an ancient hybridization process resulted in a tier of duplicated genes within its genome, many of them with implications in this ethanol "produce-accumulate-consume" strategy. The evolutionary link between ethanol production, consumption, and tolerance versus ploidy and stability of the hybrids is an ongoing debatable issue. The implication of ancestral duplicates in this metabolic rewiring, and how these duplicates differ transcriptionally, remains unsolved. Here, we study the transcriptomic adaptive signatures to ethanol as a nonfermentative carbon source to sustain clonal yeast growth by experimental evolution, emphasizing the role of duplicated genes in the adaptive process. As expected, ethanol was able to sustain growth but at a lower rate than glucose. Our results demonstrate that in asexual populations a complete transcriptomic rewiring was produced, strikingly by downregulation of duplicated genes, mainly whole-genome duplicates, whereas small-scale duplicates exhibited significant transcriptional divergence between copies. Overall, this study contributes to the understanding of evolution after gene duplication, linking transcriptional divergence with duplicates' fate in a multigene trait as ethanol tolerance.IMPORTANCE Gene duplication events have been related with increasing biological complexity through the tree of life, but also with illnesses, including cancer. Early evolutionary theories indicated that duplicated genes could explore alternative functions due to relaxation of selective constraints in one of the copies, as the other remains as ancestral-function backup. In unicellular eukaryotes like yeasts, it has been demonstrated that the fate and persistence of duplicates depend on duplication mechanism (whole-genome or small-scale events), shaping their actual genomes. Although it has been shown that small-scale duplicates tend to innovate and whole-genome duplicates specialize in ancestral functions, the implication of duplicates' transcriptional plasticity and transcriptional divergence on environmental and metabolic responses remains largely obscure. Here, by experimental adaptive evolution, we show that Saccharomyces cerevisiae is able to respond to metabolic stress (ethanol as nonfermentative carbon source) due to the persistence of duplicated genes. These duplicates respond by transcriptional rewiring, depending on their transcriptional background. Our results shed light on the mechanisms that determine the role of duplicates, and on their evolvability.

Dataset Information

Transcriptional rewiring of fungal galactose-metabolism circuitry.

Publications

Transcriptional rewiring of fungal galactose-metabolism circuitry.

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