Systematic Changes in Gene Expression Patterns Following Adaptive Evolution in Yeast

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1999 Aug 18

PMID 10449761

Citations 164

Authors

T L Ferea

D Botstein

P O Brown

R F Rosenzweig

Affiliations

Soon will be listed here.

Abstract

Culturing a population of Saccharomyces cerevisiae for many generations under conditions to which it is not optimally adapted selects for fitter genetic variants. This simple experimental design provides a tractable model of adaptive evolution under natural selection. Beginning with a clonal, founding population, independently evolved strains were obtained from three independent cultures after continuous aerobic growth in glucose-limited chemostats for more than 250 generations. DNA microarrays were used to compare genome-wide patterns of gene expression in the evolved strains and the parental strain. Several hundred genes were found to have significantly altered expression in the evolved strains. Many of these genes showed similar alterations in their expression in all three evolved strains. Genes with altered expression in the three evolved strains included genes involved in glycolysis, the tricarboxylic acid cycle, oxidative phosphorylation, and metabolite transport. These results are consistent with physiological observations and indicate that increased fitness is acquired by altering regulation of central metabolism such that less glucose is fermented and more glucose is completely oxidized.

Citing Articles

Synthetic gene circuit evolution: Insights and opportunities at the mid-scale.

Helenek C, Krzyszton R, Petreczky J, Wan Y, Cabral M, Coraci D Cell Chem Biol. 2024; 31(8):1447-1459.

PMID: 38925113 PMC: 11330362. DOI: 10.1016/j.chembiol.2024.05.018.

Evolution of Phenotypic Variance Provides Insights into the Genetic Basis of Adaptation.

Lai W, Nolte V, Jaksic A, Schlotterer C Genome Biol Evol. 2024; 16(4).

PMID: 38620076 PMC: 11057206. DOI: 10.1093/gbe/evae077.

Identifying Targets of Selection in Laboratory Evolution Experiments.

Martinez A, Lang G J Mol Evol. 2023; 91(3):345-355.

PMID: 36810618 PMC: 11197053. DOI: 10.1007/s00239-023-10096-2.

Adaptive eQTLs reveal the evolutionary impacts of pleiotropy and tissue-specificity while contributing to health and disease.

Quiver M, Lachance J HGG Adv. 2022; 3(1):100083.

PMID: 35047867 PMC: 8756519. DOI: 10.1016/j.xhgg.2021.100083.

The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast .

Mattenberger F, Fares M, Toft C, Sabater-Munoz B Int J Mol Sci. 2021; 22(22).

PMID: 34830177 PMC: 8622941. DOI: 10.3390/ijms222212293.

References

Spellman P, Sherlock G, Zhang M, Iyer V, Anders K, Eisen M . Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell. 1998; 9(12):3273-97. PMC: 25624. DOI: 10.1091/mbc.9.12.3273. View

Chu S, Derisi J, Eisen M, Mulholland J, Botstein D, Brown P . The transcriptional program of sporulation in budding yeast. Science. 1998; 282(5389):699-705. DOI: 10.1126/science.282.5389.699. View

Boyle G, Roucou X, Nagley P, Devenish R, Prescott M . Identification of subunit g of yeast mitochondrial F1F0-ATP synthase, a protein required for maximal activity of cytochrome c oxidase. Eur J Biochem. 1999; 262(2):315-23. DOI: 10.1046/j.1432-1327.1999.00345.x. View

Novick A, Szilard L . Experiments with the Chemostat on spontaneous mutations of bacteria. Proc Natl Acad Sci U S A. 1950; 36(12):708-19. PMC: 1063276. DOI: 10.1073/pnas.36.12.708. View

Horiuchi T, TOMIZAWA J, Novick A . Isolation and properties of bacteria capable of high rates of beta-galactosidase synthesis. Biochim Biophys Acta. 1962; 55:152-63. DOI: 10.1016/0006-3002(62)90941-1. View

Novick A . Growth of bacteria. Annu Rev Microbiol. 1955; 9:97-110. DOI: 10.1146/annurev.mi.09.100155.000525. View

DE DEKEN R . The Crabtree effect: a regulatory system in yeast. J Gen Microbiol. 1966; 44(2):149-56. DOI: 10.1099/00221287-44-2-149. View

Lagunas R . Energetic irrelevance of aerobiosis for S. cerevisiae growing on sugars. Mol Cell Biochem. 1979; 27(3):139-46. DOI: 10.1007/BF00215362. View

Paquin C, Adams J . Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature. 1983; 302(5908):495-500. DOI: 10.1038/302495a0. View

10.

Lagunas R . Misconceptions about the energy metabolism of Saccharomyces cerevisiae. Yeast. 1986; 2(4):221-8. DOI: 10.1002/yea.320020403. View

11.

Forsburg S, Guarente L . Identification and characterization of HAP4: a third component of the CCAAT-bound HAP2/HAP3 heteromer. Genes Dev. 1989; 3(8):1166-78. DOI: 10.1101/gad.3.8.1166. View

12.

Ulery T, Jang S, Jaehning J . Glucose repression of yeast mitochondrial transcription: kinetics of derepression and role of nuclear genes. Mol Cell Biol. 1994; 14(2):1160-70. PMC: 358472. DOI: 10.1128/mcb.14.2.1160-1170.1994. View

13.

Ronne H . Glucose repression in fungi. Trends Genet. 1995; 11(1):12-7. DOI: 10.1016/s0168-9525(00)88980-5. View

14.

DeRisi J, Iyer V, Brown P . Exploring the metabolic and genetic control of gene expression on a genomic scale. Science. 1997; 278(5338):680-6. DOI: 10.1126/science.278.5338.680. View

15.

Fox M . Some recollections and reflections on mutation rates. Genetics. 1998; 148(4):1415-8. PMC: 1460067. DOI: 10.1093/genetics/148.4.1415. View

16.

Brown C, Todd K, Rosenzweig R . Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol Biol Evol. 1998; 15(8):931-42. DOI: 10.1093/oxfordjournals.molbev.a026009. View

17.

Eisen M, Spellman P, Brown P, Botstein D . Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A. 1998; 95(25):14863-8. PMC: 24541. DOI: 10.1073/pnas.95.25.14863. View