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Posttranslational regulation impacts the fate of duplicated genes

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Abstract
Gene and genome duplications create novel genetic material on which evolution can work and have therefore been recognized as a major source of innovation for many eukaryotic lineages. Following duplication, the most likely fate is gene loss; however, a considerable fraction of duplicated genes survive. Not all genes have the same probability of survival, but it is not fully understood what evolutionary forces determine the pattern of gene retention. Here, we use genome sequence data as well as large-scale phosphoproteomics data from the baker's yeast Saccharomyces cerevisiae, which underwent a whole-genome duplication similar to 100 mya, and show that the number of phosphorylation sites on the proteins they encode is a major determinant of gene retention. Protein phosphorylation motifs are short amino acid sequences that are usually embedded within unstructured and rapidly evolving protein regions. Reciprocal loss of those ancestral sites and the gain of new ones are major drivers in the retention of the two surviving duplicates and in their acquisition of distinct functions. This way, small changes in the sequences of unstructured regions in proteins can contribute to the rapid rewiring and adaptation of regulatory networks.
Keywords
PHOSPHOPROTEOME ANALYSIS, INTERACTION NETWORK, GLOBAL ANALYSIS, EVOLUTION, YEAST, posttranslational modification, gene retention, phosphorylation, SACCHAROMYCES-CEREVISIAE GENOME, PROTEIN-PHOSPHORYLATION SITES, EXPRESSION, NEOFUNCTIONALIZATION, SUBFUNCTIONALIZATION, whole-genome duplication, gene duplication

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Citation

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MLA
Amoutzias, Grigoris, et al. “Posttranslational Regulation Impacts the Fate of Duplicated Genes.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 107, no. 7, 2010, pp. 2967–71, doi:10.1073/pnas.0911603107.
APA
Amoutzias, G., He, Y., Gordon, J., Mossialos, D., Oliver, S. G., & Van de Peer, Y. (2010). Posttranslational regulation impacts the fate of duplicated genes. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 107(7), 2967–2971. https://doi.org/10.1073/pnas.0911603107
Chicago author-date
Amoutzias, Grigoris, Ying He, Jonathan Gordon, Dimitris Mossialos, Stephen G Oliver, and Yves Van de Peer. 2010. “Posttranslational Regulation Impacts the Fate of Duplicated Genes.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 107 (7): 2967–71. https://doi.org/10.1073/pnas.0911603107.
Chicago author-date (all authors)
Amoutzias, Grigoris, Ying He, Jonathan Gordon, Dimitris Mossialos, Stephen G Oliver, and Yves Van de Peer. 2010. “Posttranslational Regulation Impacts the Fate of Duplicated Genes.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 107 (7): 2967–2971. doi:10.1073/pnas.0911603107.
Vancouver
1.
Amoutzias G, He Y, Gordon J, Mossialos D, Oliver SG, Van de Peer Y. Posttranslational regulation impacts the fate of duplicated genes. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2010;107(7):2967–71.
IEEE
[1]
G. Amoutzias, Y. He, J. Gordon, D. Mossialos, S. G. Oliver, and Y. Van de Peer, “Posttranslational regulation impacts the fate of duplicated genes,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 107, no. 7, pp. 2967–2971, 2010.
@article{912457,
  abstract     = {{Gene and genome duplications create novel genetic material on which evolution can work and have therefore been recognized as a major source of innovation for many eukaryotic lineages. Following duplication, the most likely fate is gene loss; however, a considerable fraction of duplicated genes survive. Not all genes have the same probability of survival, but it is not fully understood what evolutionary forces determine the pattern of gene retention. Here, we use genome sequence data as well as large-scale phosphoproteomics data from the baker's yeast Saccharomyces cerevisiae, which underwent a whole-genome duplication similar to 100 mya, and show that the number of phosphorylation sites on the proteins they encode is a major determinant of gene retention. Protein phosphorylation motifs are short amino acid sequences that are usually embedded within unstructured and rapidly evolving protein regions. Reciprocal loss of those ancestral sites and the gain of new ones are major drivers in the retention of the two surviving duplicates and in their acquisition of distinct functions. This way, small changes in the sequences of unstructured regions in proteins can contribute to the rapid rewiring and adaptation of regulatory networks.}},
  author       = {{Amoutzias, Grigoris and He, Ying and Gordon, Jonathan and Mossialos, Dimitris and Oliver, Stephen G and Van de Peer, Yves}},
  issn         = {{0027-8424}},
  journal      = {{PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}},
  keywords     = {{PHOSPHOPROTEOME ANALYSIS,INTERACTION NETWORK,GLOBAL ANALYSIS,EVOLUTION,YEAST,posttranslational modification,gene retention,phosphorylation,SACCHAROMYCES-CEREVISIAE GENOME,PROTEIN-PHOSPHORYLATION SITES,EXPRESSION,NEOFUNCTIONALIZATION,SUBFUNCTIONALIZATION,whole-genome duplication,gene duplication}},
  language     = {{eng}},
  number       = {{7}},
  pages        = {{2967--2971}},
  title        = {{Posttranslational regulation impacts the fate of duplicated genes}},
  url          = {{http://dx.doi.org/10.1073/pnas.0911603107}},
  volume       = {{107}},
  year         = {{2010}},
}

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