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Increased glycolytic flux as an outcome of whole-genome duplication in yeast.

Conant GC, Wolfe KH - Mol. Syst. Biol. (2007)

Bottom Line: We propose that the loss of other redundant genes throughout the genome resulted in incremental dosage increases for the surviving duplicated glycolytic genes.Because changes in gene dosage follow directly from post-WGD deletions, dosage selection can confer an almost instantaneous benefit after WGD, unlike neofunctionalization or subfunctionalization, which require specific mutations.We also show theoretically that increased fermentative capacity is of greatest advantage when glucose resources are both large and dense, an observation potentially related to the appearance of angiosperms around the time of WGD.

View Article: PubMed Central - PubMed

Affiliation: Smurfit Institute of Genetics, Trinity College, University of Dublin, Dublin, Ireland. conantg@tcd.ie

ABSTRACT
After whole-genome duplication (WGD), deletions return most loci to single copy. However, duplicate loci may survive through selection for increased dosage. Here, we show how the WGD increased copy number of some glycolytic genes could have conferred an almost immediate selective advantage to an ancestor of Saccharomyces cerevisiae, providing a rationale for the success of the WGD. We propose that the loss of other redundant genes throughout the genome resulted in incremental dosage increases for the surviving duplicated glycolytic genes. This increase gave post-WGD yeasts a growth advantage through rapid glucose fermentation; one of this lineage's many adaptations to glucose-rich environments. Our hypothesis is supported by data from enzyme kinetics and comparative genomics. Because changes in gene dosage follow directly from post-WGD deletions, dosage selection can confer an almost instantaneous benefit after WGD, unlike neofunctionalization or subfunctionalization, which require specific mutations. We also show theoretically that increased fermentative capacity is of greatest advantage when glucose resources are both large and dense, an observation potentially related to the appearance of angiosperms around the time of WGD.

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Relative growth advantage of one population over another for a range of potential resource distributions. On the x-axis is the volume of a resource patch (l); on the y-axis is the concentration of glucose (mmol/l) in that patch. The total mass of glucose is the product of the axes, but note that because metabolic rate does not scale linearly with concentration, equivalent masses of glucose at differing concentrations will give rise to differing competitive advantages. The scale indicates the ratio of the cell mass for each population when resources are exhausted. Thus, values greater than 1.0 indicate regions where a rapidly fermenting population has a competitive advantage. (A) Ratio of final cell masses between two populations, one of which has a 5% advantage in maximal fermentation rate (at a cost of ∼10% loss of efficiency in terms of grams of cell mass produced per gram of glucose consumed). (B) Comparison of a respiring and a fermenting yeast population. Blue regions (ratio<1.0) correspond to conditions under which respiration is favored; orange, where fermentation is favored.
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f4: Relative growth advantage of one population over another for a range of potential resource distributions. On the x-axis is the volume of a resource patch (l); on the y-axis is the concentration of glucose (mmol/l) in that patch. The total mass of glucose is the product of the axes, but note that because metabolic rate does not scale linearly with concentration, equivalent masses of glucose at differing concentrations will give rise to differing competitive advantages. The scale indicates the ratio of the cell mass for each population when resources are exhausted. Thus, values greater than 1.0 indicate regions where a rapidly fermenting population has a competitive advantage. (A) Ratio of final cell masses between two populations, one of which has a 5% advantage in maximal fermentation rate (at a cost of ∼10% loss of efficiency in terms of grams of cell mass produced per gram of glucose consumed). (B) Comparison of a respiring and a fermenting yeast population. Blue regions (ratio<1.0) correspond to conditions under which respiration is favored; orange, where fermentation is favored.

Mentions: We first compare two populations growing by fermentation and differing in their maximal fermentation rate. Maximal growth rates (μmaxs) were taken from van Hoek et al (1998b) as was the metabolic efficiency (the mass in grams of dry yeast cells obtained from a fixed mass of input glucose). The resource affinity Rs for respiring populations was taken from Walker (1998). Since we do not have an equivalent value for fermentatively growing yeasts, for illustrative purposes we have assumed that Rs in this case is an order of magnitude higher, similar to the difference in Km observed for the PDC and PDH enzymes (Pronk et al, 1996). Note that the exact magnitude of this difference is not critical: respiring populations will always have the selective advantage seen at lower concentrations of glucose in Figure 4B if their Rs is less than that of fermenting populations. That this is the case in real yeasts is clear from the fact that S. cerevisiae switches to respiratory growth when the concentration of glucose is sufficiently low, indicating that fermentation is not an effective growth strategy at these resource concentrations.


Increased glycolytic flux as an outcome of whole-genome duplication in yeast.

Conant GC, Wolfe KH - Mol. Syst. Biol. (2007)

Relative growth advantage of one population over another for a range of potential resource distributions. On the x-axis is the volume of a resource patch (l); on the y-axis is the concentration of glucose (mmol/l) in that patch. The total mass of glucose is the product of the axes, but note that because metabolic rate does not scale linearly with concentration, equivalent masses of glucose at differing concentrations will give rise to differing competitive advantages. The scale indicates the ratio of the cell mass for each population when resources are exhausted. Thus, values greater than 1.0 indicate regions where a rapidly fermenting population has a competitive advantage. (A) Ratio of final cell masses between two populations, one of which has a 5% advantage in maximal fermentation rate (at a cost of ∼10% loss of efficiency in terms of grams of cell mass produced per gram of glucose consumed). (B) Comparison of a respiring and a fermenting yeast population. Blue regions (ratio<1.0) correspond to conditions under which respiration is favored; orange, where fermentation is favored.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1943425&req=5

f4: Relative growth advantage of one population over another for a range of potential resource distributions. On the x-axis is the volume of a resource patch (l); on the y-axis is the concentration of glucose (mmol/l) in that patch. The total mass of glucose is the product of the axes, but note that because metabolic rate does not scale linearly with concentration, equivalent masses of glucose at differing concentrations will give rise to differing competitive advantages. The scale indicates the ratio of the cell mass for each population when resources are exhausted. Thus, values greater than 1.0 indicate regions where a rapidly fermenting population has a competitive advantage. (A) Ratio of final cell masses between two populations, one of which has a 5% advantage in maximal fermentation rate (at a cost of ∼10% loss of efficiency in terms of grams of cell mass produced per gram of glucose consumed). (B) Comparison of a respiring and a fermenting yeast population. Blue regions (ratio<1.0) correspond to conditions under which respiration is favored; orange, where fermentation is favored.
Mentions: We first compare two populations growing by fermentation and differing in their maximal fermentation rate. Maximal growth rates (μmaxs) were taken from van Hoek et al (1998b) as was the metabolic efficiency (the mass in grams of dry yeast cells obtained from a fixed mass of input glucose). The resource affinity Rs for respiring populations was taken from Walker (1998). Since we do not have an equivalent value for fermentatively growing yeasts, for illustrative purposes we have assumed that Rs in this case is an order of magnitude higher, similar to the difference in Km observed for the PDC and PDH enzymes (Pronk et al, 1996). Note that the exact magnitude of this difference is not critical: respiring populations will always have the selective advantage seen at lower concentrations of glucose in Figure 4B if their Rs is less than that of fermenting populations. That this is the case in real yeasts is clear from the fact that S. cerevisiae switches to respiratory growth when the concentration of glucose is sufficiently low, indicating that fermentation is not an effective growth strategy at these resource concentrations.

Bottom Line: We propose that the loss of other redundant genes throughout the genome resulted in incremental dosage increases for the surviving duplicated glycolytic genes.Because changes in gene dosage follow directly from post-WGD deletions, dosage selection can confer an almost instantaneous benefit after WGD, unlike neofunctionalization or subfunctionalization, which require specific mutations.We also show theoretically that increased fermentative capacity is of greatest advantage when glucose resources are both large and dense, an observation potentially related to the appearance of angiosperms around the time of WGD.

View Article: PubMed Central - PubMed

Affiliation: Smurfit Institute of Genetics, Trinity College, University of Dublin, Dublin, Ireland. conantg@tcd.ie

ABSTRACT
After whole-genome duplication (WGD), deletions return most loci to single copy. However, duplicate loci may survive through selection for increased dosage. Here, we show how the WGD increased copy number of some glycolytic genes could have conferred an almost immediate selective advantage to an ancestor of Saccharomyces cerevisiae, providing a rationale for the success of the WGD. We propose that the loss of other redundant genes throughout the genome resulted in incremental dosage increases for the surviving duplicated glycolytic genes. This increase gave post-WGD yeasts a growth advantage through rapid glucose fermentation; one of this lineage's many adaptations to glucose-rich environments. Our hypothesis is supported by data from enzyme kinetics and comparative genomics. Because changes in gene dosage follow directly from post-WGD deletions, dosage selection can confer an almost instantaneous benefit after WGD, unlike neofunctionalization or subfunctionalization, which require specific mutations. We also show theoretically that increased fermentative capacity is of greatest advantage when glucose resources are both large and dense, an observation potentially related to the appearance of angiosperms around the time of WGD.

Show MeSH
Related in: MedlinePlus