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Modeling protein network evolution under genome duplication and domain shuffling

BACKGROUND: Successive whole genome duplications have recently been firmly established in all major eukaryote kingdoms. Such exponential evolutionary processes must have largely contributed to shape the topology of protein-protein interaction (PPI) networks by outweighing, in particular, all time-li...

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Autores principales: Evlampiev, Kirill, Isambert, Hervé
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2007
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2245809/
https://www.ncbi.nlm.nih.gov/pubmed/17999763
http://dx.doi.org/10.1186/1752-0509-1-49
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author Evlampiev, Kirill
Isambert, Hervé
author_facet Evlampiev, Kirill
Isambert, Hervé
author_sort Evlampiev, Kirill
collection PubMed
description BACKGROUND: Successive whole genome duplications have recently been firmly established in all major eukaryote kingdoms. Such exponential evolutionary processes must have largely contributed to shape the topology of protein-protein interaction (PPI) networks by outweighing, in particular, all time-linear network growths modeled so far. RESULTS: We propose and solve a mathematical model of PPI network evolution under successive genome duplications. This demonstrates, from first principles, that evolutionary conservation and scale-free topology are intrinsically linked properties of PPI networks and emerge from i) prevailing exponential network dynamics under duplication and ii) asymmetric divergence of gene duplicates. While required, we argue that this asymmetric divergence arises, in fact, spontaneously at the level of protein-binding sites. This supports a refined model of PPI network evolution in terms of protein domains under exponential and asymmetric duplication/divergence dynamics, with multidomain proteins underlying the combinatorial formation of protein complexes. Genome duplication then provides a powerful source of PPI network innovation by promoting local rearrangements of multidomain proteins on a genome wide scale. Yet, we show that the overall conservation and topology of PPI networks are robust to extensive domain shuffling of multidomain proteins as well as to finer details of protein interaction and evolution. Finally, large scale features of direct and indirect PPI networks of S. cerevisiae are well reproduced numerically with only two adjusted parameters of clear biological significance (i.e. network effective growth rate and average number of protein-binding domains per protein). CONCLUSION: This study demonstrates the statistical consequences of genome duplication and domain shuffling on the conservation and topology of PPI networks over a broad evolutionary scale across eukaryote kingdoms. In particular, scale-free topologies of PPI networks, which are found to be robust to extensive shuffling of protein domains, appear to be a simple consequence of the conservation of protein-binding domains under asymmetric duplication/divergence dynamics in the course of evolution.
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spelling pubmed-22458092008-02-20 Modeling protein network evolution under genome duplication and domain shuffling Evlampiev, Kirill Isambert, Hervé BMC Syst Biol Research Article BACKGROUND: Successive whole genome duplications have recently been firmly established in all major eukaryote kingdoms. Such exponential evolutionary processes must have largely contributed to shape the topology of protein-protein interaction (PPI) networks by outweighing, in particular, all time-linear network growths modeled so far. RESULTS: We propose and solve a mathematical model of PPI network evolution under successive genome duplications. This demonstrates, from first principles, that evolutionary conservation and scale-free topology are intrinsically linked properties of PPI networks and emerge from i) prevailing exponential network dynamics under duplication and ii) asymmetric divergence of gene duplicates. While required, we argue that this asymmetric divergence arises, in fact, spontaneously at the level of protein-binding sites. This supports a refined model of PPI network evolution in terms of protein domains under exponential and asymmetric duplication/divergence dynamics, with multidomain proteins underlying the combinatorial formation of protein complexes. Genome duplication then provides a powerful source of PPI network innovation by promoting local rearrangements of multidomain proteins on a genome wide scale. Yet, we show that the overall conservation and topology of PPI networks are robust to extensive domain shuffling of multidomain proteins as well as to finer details of protein interaction and evolution. Finally, large scale features of direct and indirect PPI networks of S. cerevisiae are well reproduced numerically with only two adjusted parameters of clear biological significance (i.e. network effective growth rate and average number of protein-binding domains per protein). CONCLUSION: This study demonstrates the statistical consequences of genome duplication and domain shuffling on the conservation and topology of PPI networks over a broad evolutionary scale across eukaryote kingdoms. In particular, scale-free topologies of PPI networks, which are found to be robust to extensive shuffling of protein domains, appear to be a simple consequence of the conservation of protein-binding domains under asymmetric duplication/divergence dynamics in the course of evolution. BioMed Central 2007-11-13 /pmc/articles/PMC2245809/ /pubmed/17999763 http://dx.doi.org/10.1186/1752-0509-1-49 Text en Copyright © 2007 Evlampiev and Isambert; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( (http://creativecommons.org/licenses/by/2.0) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Evlampiev, Kirill
Isambert, Hervé
Modeling protein network evolution under genome duplication and domain shuffling
title Modeling protein network evolution under genome duplication and domain shuffling
title_full Modeling protein network evolution under genome duplication and domain shuffling
title_fullStr Modeling protein network evolution under genome duplication and domain shuffling
title_full_unstemmed Modeling protein network evolution under genome duplication and domain shuffling
title_short Modeling protein network evolution under genome duplication and domain shuffling
title_sort modeling protein network evolution under genome duplication and domain shuffling
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2245809/
https://www.ncbi.nlm.nih.gov/pubmed/17999763
http://dx.doi.org/10.1186/1752-0509-1-49
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