Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.

Gene duplications are believed to facilitate evolutionary innovation. However, the mechanisms shaping the fate of duplicated genes remain heavily debated because the molecular processes and evolutionary forces involved are difficult to reconstruct. Here, we study a large family of fungal glucosidase...

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Autores principales: Karin Voordeckers, Chris A Brown, Kevin Vanneste, Elisa van der Zande, Arnout Voet, Steven Maere, Kevin J Verstrepen
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Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2012
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Acceso en línea:https://doaj.org/article/2e6392b69ee64c7d908b29b2512328c1
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spelling oai:doaj.org-article:2e6392b69ee64c7d908b29b2512328c12021-11-18T05:37:19ZReconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.1544-91731545-788510.1371/journal.pbio.1001446https://doaj.org/article/2e6392b69ee64c7d908b29b2512328c12012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23239941/pdf/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Gene duplications are believed to facilitate evolutionary innovation. However, the mechanisms shaping the fate of duplicated genes remain heavily debated because the molecular processes and evolutionary forces involved are difficult to reconstruct. Here, we study a large family of fungal glucosidase genes that underwent several duplication events. We reconstruct all key ancestral enzymes and show that the very first preduplication enzyme was primarily active on maltose-like substrates, with trace activity for isomaltose-like sugars. Structural analysis and activity measurements on resurrected and present-day enzymes suggest that both activities cannot be fully optimized in a single enzyme. However, gene duplications repeatedly spawned daughter genes in which mutations optimized either isomaltase or maltase activity. Interestingly, similar shifts in enzyme activity were reached multiple times via different evolutionary routes. Together, our results provide a detailed picture of the molecular mechanisms that drove divergence of these duplicated enzymes and show that whereas the classic models of dosage, sub-, and neofunctionalization are helpful to conceptualize the implications of gene duplication, the three mechanisms co-occur and intertwine.Karin VoordeckersChris A BrownKevin VannesteElisa van der ZandeArnout VoetSteven MaereKevin J VerstrepenPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 10, Iss 12, p e1001446 (2012)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
Karin Voordeckers
Chris A Brown
Kevin Vanneste
Elisa van der Zande
Arnout Voet
Steven Maere
Kevin J Verstrepen
Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.
description Gene duplications are believed to facilitate evolutionary innovation. However, the mechanisms shaping the fate of duplicated genes remain heavily debated because the molecular processes and evolutionary forces involved are difficult to reconstruct. Here, we study a large family of fungal glucosidase genes that underwent several duplication events. We reconstruct all key ancestral enzymes and show that the very first preduplication enzyme was primarily active on maltose-like substrates, with trace activity for isomaltose-like sugars. Structural analysis and activity measurements on resurrected and present-day enzymes suggest that both activities cannot be fully optimized in a single enzyme. However, gene duplications repeatedly spawned daughter genes in which mutations optimized either isomaltase or maltase activity. Interestingly, similar shifts in enzyme activity were reached multiple times via different evolutionary routes. Together, our results provide a detailed picture of the molecular mechanisms that drove divergence of these duplicated enzymes and show that whereas the classic models of dosage, sub-, and neofunctionalization are helpful to conceptualize the implications of gene duplication, the three mechanisms co-occur and intertwine.
format article
author Karin Voordeckers
Chris A Brown
Kevin Vanneste
Elisa van der Zande
Arnout Voet
Steven Maere
Kevin J Verstrepen
author_facet Karin Voordeckers
Chris A Brown
Kevin Vanneste
Elisa van der Zande
Arnout Voet
Steven Maere
Kevin J Verstrepen
author_sort Karin Voordeckers
title Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.
title_short Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.
title_full Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.
title_fullStr Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.
title_full_unstemmed Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.
title_sort reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/2e6392b69ee64c7d908b29b2512328c1
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AT chrisabrown reconstructionofancestralmetabolicenzymesrevealsmolecularmechanismsunderlyingevolutionaryinnovationthroughgeneduplication
AT kevinvanneste reconstructionofancestralmetabolicenzymesrevealsmolecularmechanismsunderlyingevolutionaryinnovationthroughgeneduplication
AT elisavanderzande reconstructionofancestralmetabolicenzymesrevealsmolecularmechanismsunderlyingevolutionaryinnovationthroughgeneduplication
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