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Questioning the Ubiquity of Neofunctionalization

DOI: 10.1371/journal.pcbi.1000252

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Abstract:

Gene duplication provides much of the raw material from which functional diversity evolves. Two evolutionary mechanisms have been proposed that generate functional diversity: neofunctionalization, the de novo acquisition of function by one duplicate, and subfunctionalization, the partitioning of ancestral functions between gene duplicates. With protein interactions as a surrogate for protein functions, evidence of prodigious neofunctionalization and subfunctionalization has been identified in analyses of empirical protein interactions and evolutionary models of protein interactions. However, we have identified three phenomena that have contributed to neofunctionalization being erroneously identified as a significant factor in protein interaction network evolution. First, self-interacting proteins are underreported in interaction data due to biological artifacts and design limitations in the two most common high-throughput protein interaction assays. Second, evolutionary inferences have been drawn from paralog analysis without consideration for concurrent and subsequent duplication events. Third, the theoretical model of prodigious neofunctionalization is unable to reproduce empirical network clustering and relies on untenable parameter requirements. In light of these findings, we believe that protein interaction evolution is more persuasively characterized by subfunctionalization and self-interactions.

References

[1]  Ohno S (1970) Evolution by Gene Duplication. New York: Springer.
[2]  Force A, Lynch M, Pickett FB, Amores A, Yan YL, et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531–1545.
[3]  Wagner A (2001) The yeast protein interaction network evolves rapidly and contains few redundant duplicate genes. Mol Biol Evol 18: 1283–1292.
[4]  Wagner A (2003) How the global structure of protein interaction networks evolves. Proc Biol Sci 270: 457–466.
[5]  Beltrao P, Serrano L (2007) Specificity and evolvability in eukaryotic protein interaction networks. PLoS Comput Biol 3: e25. doi:10.1371/journal.pcbi.0030025.
[6]  He X, Zhang J (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169: 1157–1164.
[7]  Solé RV, Pastor-Satorras R, Smith E, Kepler TB (2002) A model of large-scale proteome evolution. Adv Complex Syst 5: 43.
[8]  Pereira-Leal J, Levy E, Kamp C, Teichmann S (2007) Evolution of protein complexes by duplication of homomeric interactions. Genome Biol 8: R51.
[9]  Ispolatov I, Yuryev A, Mazo I, Maslov S (2005) Binding properties and evolution of homodimers in protein–protein interaction networks. Nucleic Acids Res 33: 3629–3635.
[10]  Carey M, Kakidani H, Leatherwood J, Mostashari F, Ptashne M (1989) An amino-terminal fragment of GAL4 binds DNA as a dimer. J Mol Biol 209: 423–432.
[11]  Marmorstein R, Carey M, Ptashne M, Harrison SC (1992) DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356: 408–414.
[12]  Newman JR, Wolf E, Kim PS (2000) A computationally directed screen identifying interacting coiled coils from Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 97: 13203–13208.
[13]  Hu JC (2000) A guided tour in protein interaction space: coiled coils from the yeast proteome. Proc Natl Acad Sci U S A 97: 12935–12936.
[14]  Gavin AC, Bsche M, Krause R, Grandi P, Marzioch M, et al. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141–147.
[15]  Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, et al. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631–636.
[16]  Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, et al. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637–643.
[17]  Gavin AC Personal communication.
[18]  Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, et al. (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415: 180–183.
[19]  Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235–242.
[20]  Finn RD, Marshall M, Bateman A (2005) iPfam: visualization of protein-protein interactions in PDB at domain and amino acid resolutions. Bioinformatics 21: 410–412.
[21]  Schomburg I, Chang A, Ebeling C, Gremse M, Heldt C, et al. (2004) BRENDA, the enzyme database: updates and major new developments. Nucleic Acids Res 32: D431–D433.
[22]  Pereira-Leal JB, Levy ED, Teichmann SA (2006) The origins and evolution of functional modules: lessons from protein complexes. Philos Trans R Soc Lond B Biol Sci 361: 507–517.
[23]  Henrick K, Thornton JM (1998) PQS: a protein quaternary structure file server. Trends Biochem Sci 23: 358–361.
[24]  Zhang LV, Wong SL, King OD, Roth FP (2004) Predicting co-complexed protein pairs using genomic and proteomic data integration. BMC Bioinformatics 5: 38.
[25]  Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, et al. (2000) A comprehensive analysis of protein–protein interactions in Saccharomyces cerevisiae. Nature 403: 623–627.
[26]  Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, et al. (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci U S A 98: 4569–4574.
[27]  Mewes HW, Heumann K, Kaps A, Mayer K, Pfeiffer F, et al. (1999) MIPS: a database for genomes and protein sequences. Nucleic Acids Res 27: 44–48.
[28]  Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54–61.
[29]  Mewes HW, Frishman D, Mayer KFX, Mnsterktter M, Noubibou O, et al. (2006) MIPS: analysis and annotation of proteins from whole genomes in 2005. Nucleic Acids Res 34: D169–D172.
[30]  von Mering C, Krause R, Snel B, Cornell M, Oliver SG, et al. (2002) Comparative assessment of large-scale data sets of protein-protein interactions. Nature 417: 399–403.
[31]  Stark C, Breitkreutz BJ, Reguly T, Boucher L, Breitkreutz A, et al. (2006) BioGRID: a general repository for interaction datasets. Nucleic Acids Res 34: D535–D539.
[32]  Vázquez A, Flammini A, Maritan A, Vespignani A (2003) Modeling of protein interaction networks. ComPlexUs 1: 38–44.
[33]  Newman ME (2001) The structure of scientific collaboration networks. Proc Natl Acad Sci U S A 98: 404–409.
[34]  Goldberg DS, Roth FP (2003) Assessing experimentally derived interactions in a small world. Proc Natl Acad Sci U S A 100: 4372–4376.
[35]  Yook SH, Oltvai ZN, Barabási AL (2004) Functional and topological characterization of protein interaction networks. Proteomics 4: 928–942.
[36]  Han JDJ, Dupuy D, Bertin N, Cusick ME, Vidal M (2005) Effect of sampling on topology predictions of protein-protein interaction networks. Nat Biotechnol 23: 839–844.
[37]  Tarassov K, Messier V, Landry CR, Radinovic S, Molina MMS, et al. (2008) An in vivo map of the yeast protein interactome. Science 320: 1465–1470.
[38]  Batada NN, Reguly T, Breitkreutz A, Boucher L, Breitkreutz BJ, et al. (2007) Still stratus not altocumulus: further evidence against the date/party hub distinction. PLoS Biol 5: e154. doi:10.1371/journal.pbio.0050154.
[39]  Kiemer L, Costa S, Ueffing M, Cesareni G (2007) Wi-phi: a weighted yeast interactome enriched for direct physical interactions. Proteomics 7: 932–943.
[40]  Collins SR, Kemmeren P, Zhao XC, Greenblatt JF, Spencer F, et al. (2007) Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol Cell Proteomics 6: 439–450.
[41]  Hakes L, Robertson DL, Oliver SG (2005) Effect of dataset selection on the topological interpretation of protein interaction networks. BMC Genomics 6: 131.
[42]  Coulomb S, Bauer M, Bernard D, Marsolier-Kergoat MC (2005) Gene essentiality and the topology of protein interaction networks. Proc Biol Sci 272: 1721–1725.
[43]  Stumpf MPH, Wiuf C, May RM (2005) Subnets of scale-free networks are not scale-free: sampling properties of networks. Proc Natl Acad Sci U S A 102: 4221–4224.
[44]  Presser A, Elowitz MB, Kellis M, Kishony R (2008) The evolutionary dynamics of the saccharomyces cerevisiae protein interaction network after duplication. Proc Natl Acad Sci U S A 105: 950–954.
[45]  Berg J, L?ssig M, Wagner A (2004) Structure and evolution of protein interaction networks: a statistical model for link dynamics and gene duplications. BMC Evol Biol 4: 51.
[46]  Maslov S, Sneppen K, Eriksen KA, Yan KK (2004) Upstream plasticity and downstream robustness in evolution of molecular networks. BMC Evol Biol 4: 9.
[47]  Chung WY, Albert R, Albert I, Nekrutenko A, Makova KD (2006) Rapid and asymmetric divergence of duplicate genes in the human gene coexpression network. BMC Bioinformatics 7: 46.
[48]  Friedel CC, Zimmer R (2006) Inferring topology from clustering coefficients in protein-protein interaction networks. BMC Bioinformatics 7: 519.
[49]  Jeong H, Mason SP, Barabási AL, Oltvai ZN (2001) Lethality and centrality in protein networks. Nature 411: 41–42.
[50]  Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296: 910–913.
[51]  Milo R, Kashtan N, Itzkovitz S, Newman M, Alon U (2004) On the uniform generation of random graphs with prescribed degree sequences. http://aps.arxiv.org/abs/cond-mat/031202?8/.
[52]  Middendorf M, Ziv E, Wiggins CH (2005) Inferring network mechanisms: the Drosophila melanogaster protein interaction network. Proc Natl Acad Sci U S A 102: 3192–3197.
[53]  Ispolatov I, Krapivsky PL, Mazo I, Yuryev A (2005) Cliques and duplication–divergence network growth. New J Phys 7: 145.
[54]  Hormozdiari F, Berenbrink P, Pr?ulj N, Sahinalp SC (2007) Not all scale-free networks are born equal: The role of the seed graph in PPI network evolution. PLoS Comput Biol 3: e118. doi:10.1371/journal.pcbi.0030118.
[55]  Long M, Betrn E, Thornton K, Wang W (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4: 865–875.
[56]  Bornberg-Bauer E, Beaussart F, Kummerfeld SK, Teichmann SA, Weiner J (2005) The evolution of domain arrangements in proteins and interaction networks. Cell Mol Life Sci 62: 435–445.
[57]  Levy ED, Pereira-Leal JB, Chothia C, Teichmann SA (2006) 3D complex: a structural classification of protein complexes. PLoS Comput Biol 2: e155. doi:10.1371/journal.pcbi.0020155.
[58]  Cordella LP, Foggia P, Sansone C, Vento M (2004) A (sub)graph isomorphism algorithm for matching large graphs. IEEE Trans Pattern Anal Mach Intell 26: 1367–1372.

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