Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment.

When microbes evolve in a continuous, nutrient-limited environment, natural selection can be predicted to favor genetic changes that give cells greater access to limiting substrate. We analyzed a population of baker's yeast that underwent 450 generations of glucose-limited growth. Relative to the strain used as the inoculum, the predominant cell type at the end of this experiment sustains growth at significantly lower steady-state glucose concentrations and demonstrates markedly enhanced cell yield per mole glucose, significantly enhanced high-affinity glucose transport, and greater relative fitness in pairwise competition. These changes are correlated with increased levels of mRNA hybridizing to probe generated from the hexose transport locus HXT6. Further analysis of the evolved strain reveals the existence of multiple tandem duplications involving two highly similar, high-affinity hexose transport loci, HXT6 and HXT7. Selection appears to have favored changes that result in the formation of more than three chimeric genes derived from the upstream promoter of the HXT7 gene and the coding sequence of HXT6. We propose a genetic mechanism to account for these changes and speculate as to their adaptive significance in the context of gene duplication as a common response of microorganisms to nutrient limitation.

[1]  H. Liang,et al.  A novel signal transduction pathway in Saccharomyces cerevisiae defined by Snf3-regulated expression of HXT6. , 1996, Molecular biology of the cell.

[2]  A. Kruckeberg,et al.  The hexose transporter family of Saccharomyces cerevisiae , 1996, Archives of Microbiology.

[3]  B. Barrell,et al.  Life with 6000 Genes , 1996, Science.

[4]  R. Lenski,et al.  Punctuated Evolution Caused by Selection of Rare Beneficial Mutations , 1996, Science.

[5]  M Travisano,et al.  Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. , 1996, Genetics.

[6]  B E Wright,et al.  The effect of the stringent response on mutation rates in Escherichia coli K‐12 , 1996, Molecular microbiology.

[7]  J. Shapiro,et al.  The significances of bacterial colony patterns , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[8]  M. Ciriacy,et al.  Identification of novel HXT genes in Saccharomyces cerevisiae reveals the impact of individual hexose transporters on qlycolytic flux , 1995, Molecular microbiology.

[9]  M. Johnston,et al.  Three different regulatory mechanisms enable yeast hexose transporter (HXT) genes to be induced by different levels of glucose , 1995, Molecular and cellular biology.

[10]  A. F. Bennett,et al.  Experimental tests of the roles of adaptation, chance, and history in evolution. , 1995, Science.

[11]  R. Lenski,et al.  Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. Rosenzweig,et al.  Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. , 1994, Genetics.

[13]  L. Bisson,et al.  High-copy suppression of glucose transport defects by HXT4 and regulatory elements in the promoters of the HXT genes in Saccharomyces cerevisiae. , 1994, Genetics.

[14]  R. Lenski,et al.  Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Saunders Population Genetics of bacteria. , 1994 .

[16]  Gerald R. Fink,et al.  Guide to yeast genetics and molecular biology , 1993 .

[17]  R. Lenski,et al.  The directed mutation controversy and neo-Darwinism. , 1993, Science.

[18]  B. Hall Selection-induced mutations occur in yeast. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[19]  F. Sherman Getting started with yeast. , 1991, Methods in enzymology.

[20]  D. Dykhuizen,et al.  Enzyme activity and fitness: Evolution in solution. , 1990, Trends in ecology & evolution.

[21]  A. Dean Selection and neutrality in lactose operons of Escherichia coli. , 1989, Genetics.

[22]  J. Adams,et al.  Evolution of Escherichia coli during growth in a constant environment. , 1987, Genetics.

[23]  D. Hartl,et al.  Metabolic flux and fitness. , 1987, Genetics.

[24]  D. Hartl,et al.  Limits of adaptation: the evolution of selective neutrality. , 1985, Genetics.

[25]  A. Hinnen,et al.  Structural analysis of the two tandemly repeated acid phosphatase genes in yeast. , 1984, Nucleic acids research.

[26]  B. Hall The Evolved β-Galactosidase System of Escherichia coli , 1984 .

[27]  R. Mortlock Microorganisms as Model Systems for Studying Evolution , 1984, Monographs in Evolutionary Biology.

[28]  C. Paquin,et al.  Relative fitness can decrease in evolving asexual populations of S. cerevisiae , 1983, Nature.

[29]  C. Paquin,et al.  Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations , 1983, Nature.

[30]  L. Bisson,et al.  Involvement of kinases in glucose and fructose uptake by Saccharomyces cerevisiae. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[31]  R. Seidel,et al.  Molecular cloning of the actin gene from yeast Saccharomyces cerevisiae. , 1980, Nucleic acids research.

[32]  G. Fink,et al.  Methods in yeast genetics , 1979 .

[33]  P. Lange,et al.  Gene duplication in Saccharomyces cerevisiae. , 1978, Genetics.

[34]  E. Southern Detection of specific sequences among DNA fragments separated by gel electrophoresis. , 1975, Journal of molecular biology.

[35]  P. Hansche,et al.  Gene duplication as a mechanism of genetic adaptation in Saccharomyces cerevisiae. , 1975, Genetics.

[36]  J. C. Francis,et al.  Directed evolution of metabolic pathways in microbial populations. I. Modification of the acid phosphatase pH optimum in S. cerevisiae. , 1972, Genetics.

[37]  A. H. Rose Energy-Yielding Metabolism , 1968 .

[38]  A. Novick,et al.  The genetic basis of hyper-synthesis of beta-galactosidase. , 1963, Genetics.

[39]  A. Novick,et al.  Isolation and properties of bacteria capable of high rates of β-galactosidase synthesis , 1962 .

[40]  J. Monod,et al.  Recherches sur la croissance des cultures bactériennes , 1942 .