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

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...

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Main Authors: Gavin C Conant, Kenneth H Wolfe
Format: Article
Language:English
Published: Springer Nature 2007-07-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb4100170
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author Gavin C Conant
Kenneth H Wolfe
author_facet Gavin C Conant
Kenneth H Wolfe
author_sort Gavin C Conant
collection DOAJ
description 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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spelling doaj-art-53700265ae574635a0072e84eddafd262025-08-24T12:02:07ZengSpringer NatureMolecular Systems Biology1744-42922007-07-013111210.1038/msb4100170Increased glycolytic flux as an outcome of whole‐genome duplication in yeastGavin C Conant0Kenneth H Wolfe1Smurfit Institute of Genetics, Trinity College, University of DublinSmurfit Institute of Genetics, Trinity College, University of DublinAbstract 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.https://doi.org/10.1038/msb4100170evolutiongenome duplicationmetabolism
spellingShingle Gavin C Conant
Kenneth H Wolfe
Increased glycolytic flux as an outcome of whole‐genome duplication in yeast
Molecular Systems Biology
evolution
genome duplication
metabolism
title Increased glycolytic flux as an outcome of whole‐genome duplication in yeast
title_full Increased glycolytic flux as an outcome of whole‐genome duplication in yeast
title_fullStr Increased glycolytic flux as an outcome of whole‐genome duplication in yeast
title_full_unstemmed Increased glycolytic flux as an outcome of whole‐genome duplication in yeast
title_short Increased glycolytic flux as an outcome of whole‐genome duplication in yeast
title_sort increased glycolytic flux as an outcome of whole genome duplication in yeast
topic evolution
genome duplication
metabolism
url https://doi.org/10.1038/msb4100170
work_keys_str_mv AT gavincconant increasedglycolyticfluxasanoutcomeofwholegenomeduplicationinyeast
AT kennethhwolfe increasedglycolyticfluxasanoutcomeofwholegenomeduplicationinyeast