Roles of cis- and trans-changes in the regulatory evolution of genes in the gluconeogenic pathway in yeast

Ya Wen Chang, Fu Guo Robert Liu, Ning Yu, Huang-Mo Sung, Peggy Yang, Daryi Wang, Chih Jen Huang, Ming Che Shih, Wen Hsiung Li

Research output: Contribution to journalArticle

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Abstract

The yeast Saccharomyces cerevisiae proliferates rapidly in glucose-containing media. As glucose is getting depleted, yeast cells enter the transition from fermentative to nonfermentative metabolism, known as the diauxic shift, which is associated with major changes in gene expression. To understand the expression evolution of genes involved in the diauxic shift and in nonfermentative metabolism within species, a laboratory strain (BY), a wild strain (RM), and a clinical isolate (YJM) were used in this study. Our data showed that the RM strain enters into the diauxic shift ∼1 h earlier than the BY strain with an earlier, higher induction of many key transcription factors (TFs) involved in the diauxic shift. Our sequence data revealed sequence variations between BY and RM in both coding and promoter regions of the majority of these TFs. The key TF Cat8p, a zinc-finger cluster protein, is required for the expression of many genes in gluconeogenesis under nonfermentative growth, and its derepression is mediated by deactivation of Mig1p. Our kinetic study of CAT8 expression revealed that CAT8 induction corresponded to the timing of glucose depletion in both BY and RM and CAT8 was induced up to 50- to 90-folds in RM, whereas only 20- to 30-folds in BY. In order to decipher the relative importance of cis- and trans-variations in expression divergence in the gluconeogenic pathway during the diauxic shift, we studied the expression levels of MIG1, CAT8, and their downstream target genes in the cocultures and in the hybrid diploids of BY-RM, BY-YJM, and RM-YJM and in strains with swapped promoters. Our data showed that the differences between BY and RM in the expression of MIG1, the upstream regulator of CAT8, were affected mainly by changes in cis-elements, though also by changes in trans-acting factors, whereas those of CAT8 and its downstream target genes were predominantly affected by changes in trans-acting factors.

Original languageEnglish
Pages (from-to)1863-1875
Number of pages13
JournalMolecular Biology and Evolution
Volume25
Issue number9
DOIs
Publication statusPublished - 2008 Sep 1

Fingerprint

Regulator Genes
yeast
Transcription Factors
Trans-Activators
Yeasts
yeasts
Gene Expression
Glucose
glucose
gene
transcription factors
Gluconeogenesis
genes
metabolism
Zinc Fingers
Coculture Techniques
fold
Diploidy
Genetic Promoter Regions
Genes

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

Cite this

Chang, Ya Wen ; Robert Liu, Fu Guo ; Yu, Ning ; Sung, Huang-Mo ; Yang, Peggy ; Wang, Daryi ; Huang, Chih Jen ; Shih, Ming Che ; Li, Wen Hsiung. / Roles of cis- and trans-changes in the regulatory evolution of genes in the gluconeogenic pathway in yeast. In: Molecular Biology and Evolution. 2008 ; Vol. 25, No. 9. pp. 1863-1875.
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abstract = "The yeast Saccharomyces cerevisiae proliferates rapidly in glucose-containing media. As glucose is getting depleted, yeast cells enter the transition from fermentative to nonfermentative metabolism, known as the diauxic shift, which is associated with major changes in gene expression. To understand the expression evolution of genes involved in the diauxic shift and in nonfermentative metabolism within species, a laboratory strain (BY), a wild strain (RM), and a clinical isolate (YJM) were used in this study. Our data showed that the RM strain enters into the diauxic shift ∼1 h earlier than the BY strain with an earlier, higher induction of many key transcription factors (TFs) involved in the diauxic shift. Our sequence data revealed sequence variations between BY and RM in both coding and promoter regions of the majority of these TFs. The key TF Cat8p, a zinc-finger cluster protein, is required for the expression of many genes in gluconeogenesis under nonfermentative growth, and its derepression is mediated by deactivation of Mig1p. Our kinetic study of CAT8 expression revealed that CAT8 induction corresponded to the timing of glucose depletion in both BY and RM and CAT8 was induced up to 50- to 90-folds in RM, whereas only 20- to 30-folds in BY. In order to decipher the relative importance of cis- and trans-variations in expression divergence in the gluconeogenic pathway during the diauxic shift, we studied the expression levels of MIG1, CAT8, and their downstream target genes in the cocultures and in the hybrid diploids of BY-RM, BY-YJM, and RM-YJM and in strains with swapped promoters. Our data showed that the differences between BY and RM in the expression of MIG1, the upstream regulator of CAT8, were affected mainly by changes in cis-elements, though also by changes in trans-acting factors, whereas those of CAT8 and its downstream target genes were predominantly affected by changes in trans-acting factors.",
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Chang, YW, Robert Liu, FG, Yu, N, Sung, H-M, Yang, P, Wang, D, Huang, CJ, Shih, MC & Li, WH 2008, 'Roles of cis- and trans-changes in the regulatory evolution of genes in the gluconeogenic pathway in yeast', Molecular Biology and Evolution, vol. 25, no. 9, pp. 1863-1875. https://doi.org/10.1093/molbev/msn138

Roles of cis- and trans-changes in the regulatory evolution of genes in the gluconeogenic pathway in yeast. / Chang, Ya Wen; Robert Liu, Fu Guo; Yu, Ning; Sung, Huang-Mo; Yang, Peggy; Wang, Daryi; Huang, Chih Jen; Shih, Ming Che; Li, Wen Hsiung.

In: Molecular Biology and Evolution, Vol. 25, No. 9, 01.09.2008, p. 1863-1875.

Research output: Contribution to journalArticle

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AU - Chang, Ya Wen

AU - Robert Liu, Fu Guo

AU - Yu, Ning

AU - Sung, Huang-Mo

AU - Yang, Peggy

AU - Wang, Daryi

AU - Huang, Chih Jen

AU - Shih, Ming Che

AU - Li, Wen Hsiung

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