Functional diversification of duplicate genes through subcellular adaptation of encoded proteins

Ana C Marques , Nicolas Vinckenbosch , David Brawand and Henrik Kaessmann

Center for Integrative Genomics, University of Lausanne, CH-1015 Lausanne, Switzerland

author email corresponding author email

Genome Biology 2008, 9:R54doi:10.1186/gb-2008-9-3-r54


Published:	12 March 2008

Subject areas: Genetics, Genome studies, Evolution, Microbiology and parasitology, Model organisms

Abstract

Background

Gene duplication is the primary source of new genes with novel or altered functions. It is known that duplicates may obtain these new functional roles by evolving divergent expression patterns and/or protein functions after the duplication event. Here, using yeast (Saccharomyces cerevisiae) as a model organism, we investigate a previously little considered mode for the functional diversification of duplicate genes: subcellular adaptation of encoded proteins.

Results

We show that for 24-37% of duplicate gene pairs derived from the S. cerevisiae whole-genome duplication event, the two members of the pair encode proteins that localize to distinct subcellular compartments. The propensity of yeast duplicate genes to evolve new localization patterns depends to a large extent on the biological function of their progenitor genes. Proteins involved in processes with a wider subcellular distribution (for example, catabolism) frequently evolved new protein localization patterns after duplication, whereas duplicate proteins limited to a smaller number of organelles (for example, highly expressed biosynthesis/housekeeping proteins with a slow rate of evolution) rarely relocate within the cell. Paralogous proteins evolved divergent localization patterns by partitioning of ancestral localizations ('sublocalization'), but probably more frequently by relocalization to new compartments ('neolocalization'). We show that such subcellular reprogramming may occur through selectively driven substitutions in protein targeting sequences. Notably, our data also reveal that relocated proteins functionally adapted to their new subcellular environments and evolved new functional roles through changes of their physico-chemical properties, expression levels, and interaction partners.

Conclusion

We conclude that protein subcellular adaptation represents a common mechanism for the functional diversification of duplicate genes.