Posttranslational regulation impacts the fate of duplicated genes
Grigoris D. Amoutzias a,b,1, Ying He a,b,1, Jonathan Gordon a,b, Dimitris Mossialos c, Stephen G. Oliver d,2 and Yves Van de Peer a,b,3
- Author Affiliations
aDepartment of Plant Systems Biology, Flanders Institute for Biotechnology, 9052 Ghent, Belgium
bDepartment of Molecular Genetics, Ghent University, 9052 Ghent, Belgium
cDepartment of Biochemistry and Biotechnology, University of Thessaly, Larissa GR 41221, Greece
dCambridge Systems Biology Centre and Department of Biochemistry, University of Cambridge, Cambridge CB2 1GA, United Kingdom
Edited by Marc C. E. Van Montagu, Ghent University, Ghent, Belgium, and approved November 17, 2009 (received for review October 8, 2009)
↵1 G.D.A. and Y.H. contributed equally to this work.
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 ∼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.
gene duplication whole-genome duplication gene retention phosphorylation posttranslational modification
Footnotes
2To whom correspondence may be addressed at: Cambridge Systems Biology Centre and Department of Biochemistry, University of Cambridge, Sanger Building, 80 Tennis Court Road, Cambridge CB2 1GA, United Kingdom. E-mail: steve.oliver@bioc.cam.ac.uk.
3To whom correspondence may be addressed at: Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB), 9052 Ghent, Belgium. E-mail: yves.vandepeer@psb.vib-ugent.be.
Author contributions: G.D.A., D.M., S.G.O., and Y.V.d.P. designed research; G.D.A., Y.H., and J.G. performed research; G.D.A., Y.H., and J.G. analyzed data; and G.D.A., S.G.O., and Y.V.d.P. wrote the paper.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/cgi/content/full/0911603107/DCSupplemental.
This article is a PNAS Direct Submission.
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