The evolution of multimeric protein assemblages.

Although the mechanisms by which complex cellular features evolve constitute one of the great unsolved problems of evolutionary biology, it is clear that the emergence of new protein-protein interactions, often accompanied by the diversification of duplicate genes, is involved. Using information on the levels of protein multimerization in major phylogenetic groups as a guide to the patterns that must be explained and relying on results from population-genetic theory to define the relative plausibility of alternative evolutionary pathways, a framework for understanding the evolution of dimers is developed. The resultant theory demonstrates that the likelihoods of alternative pathways for the emergence of protein complexes depend strongly on the effective population size. Nonetheless, it is equally clear that further advancements in this area will require comparative studies on the fitness consequences of alternative monomeric and dimeric proteins.

[1]  J. B. Spofford Heterosis and the Evolution of Duplications , 1969, The American Naturalist.

[2]  A. Force,et al.  Preservation of duplicate genes by complementary, degenerative mutations. , 1999, Genetics.

[3]  R B Loftfield,et al.  The frequency of errors in protein biosynthesis. , 1972, The Biochemical journal.

[4]  D. Bedwell,et al.  Discrimination between defects in elongation fidelity and termination efficiency provides mechanistic insights into translational readthrough. , 2005, Journal of molecular biology.

[5]  L. Amos,et al.  Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. , 2009, The international journal of biochemistry & cell biology.

[6]  J. B. Walsh,et al.  How often do duplicated genes evolve new functions? , 1995, Genetics.

[7]  Martijn A. Huynen,et al.  Reconstructing the evolution of the mitochondrial ribosomal proteome , 2007, Nucleic acids research.

[8]  Fabrizio Chiti,et al.  Amyloid formation by globular proteins under native conditions. , 2009, Nature chemical biology.

[9]  Nigel F. Delaney,et al.  Darwinian Evolution Can Follow Only Very Few Mutational Paths to Fitter Proteins , 2006, Science.

[10]  Ben Lehner,et al.  Intrinsic Protein Disorder and Interaction Promiscuity Are Widely Associated with Dosage Sensitivity , 2009, Cell.

[11]  David Baker,et al.  Emergence of symmetry in homooligomeric biological assemblies , 2008, Proceedings of the National Academy of Sciences.

[12]  T. Kunkel,et al.  DNA mismatch repair. , 2005, Annual review of biochemistry.

[13]  M. Fares,et al.  Testing the neutral fixation of hetero-oligomerism in the archaeal chaperonin CCT. , 2007, Molecular biology and evolution.

[14]  Steven Henikoff,et al.  Phylogenomics of the nucleosome , 2003, Nature Structural Biology.

[15]  S. Frank Title Maladaptation and the Paradox of Robustness in Evolution Permalink , 2007 .

[16]  J. Matthews,et al.  The power of two: protein dimerization in biology. , 2004, Trends in biochemical sciences.

[17]  J M Thornton,et al.  Protein-protein interactions: a review of protein dimer structures. , 1995, Progress in biophysics and molecular biology.

[18]  John Kuriyan,et al.  The origin of protein interactions and allostery in colocalization , 2007, Nature.

[19]  A. Stoltzfus On the Possibility of Constructive Neutral Evolution , 1999, Journal of Molecular Evolution.

[20]  A. Hughes The evolution of functionally novel proteins after gene duplication , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  Michael W. Gray,et al.  Irremediable Complexity? , 2010, Science.

[22]  P. Modrich,et al.  DNA Mismatch Repair: Functions and Mechanisms , 2006 .

[23]  Douglas G. Scofield,et al.  Evolutionary diversification of the Sm family of RNA-associated proteins. , 2008, Molecular biology and evolution.

[24]  J. Dent The evolution of pentameric ligand-gated ion channels. , 2010, Advances in experimental medicine and biology.

[25]  J. Buchanan,et al.  Accuracy of in vitro protein synthesis: Translation of polyuridylic acid by cell-free extracts of human fibroblasts , 1980, Mechanisms of Ageing and Development.

[26]  A. Force,et al.  The probability of preservation of a newly arisen gene duplicate. , 2001, Genetics.

[27]  C. Holt,et al.  Subcellular mRNA Localization in Animal Cells and Why It Matters , 2009, Science.

[28]  D. Petrov,et al.  Evidence That Mutation Is Universally Biased towards AT in Bacteria , 2010, PLoS genetics.

[29]  Matthew W. Hahn,et al.  Pervasive Multinucleotide Mutational Events in Eukaryotes , 2011, Current Biology.

[30]  Daniel B. Weissman,et al.  The Rate of Fitness-Valley Crossing in Sexual Populations , 2010, Genetics.

[31]  A. Force,et al.  The probability of duplicate gene preservation by subfunctionalization. , 2000, Genetics.

[32]  J. Huntington Serpin structure, function and dysfunction , 2011, Journal of thrombosis and haemostasis : JTH.

[33]  M. Lynch,et al.  On the formation of novel genes by duplication in the Caenorhabditis elegans genome. , 2006, Molecular biology and evolution.

[34]  S. Gygi,et al.  Fission yeast SWI/SNF and RSC complexes show compositional and functional differences from budding yeast , 2008, Nature Structural &Molecular Biology.

[35]  M. DePristo,et al.  Mutational reversions during adaptive protein evolution. , 2007, Molecular biology and evolution.

[36]  W. Doolittle,et al.  How a neutral evolutionary ratchet can build cellular complexity , 2011, IUBMB life.

[37]  C Chothia,et al.  Surface, subunit interfaces and interior of oligomeric proteins. , 1988, Journal of molecular biology.

[38]  Sarah A. Teichmann,et al.  3D Complex: A Structural Classification of Protein Complexes , 2006, PLoS Comput. Biol..

[39]  P. Farabaugh,et al.  The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. , 2006, RNA.

[40]  M. Abramowitz,et al.  Handbook of Mathematical Functions With Formulas, Graphs and Mathematical Tables (National Bureau of Standards Applied Mathematics Series No. 55) , 1965 .

[41]  E I Shakhnovich,et al.  Structural similarity enhances interaction propensity of proteins. , 2006, Journal of molecular biology.

[42]  Sarah A Teichmann,et al.  Evolution of protein complexes by duplication of homomeric interactions , 2007, Genome Biology.

[43]  Simone Campanoni Competition , 1866, Nature.

[44]  B. Shraiman,et al.  Genetic Draft and Quasi-Neutrality in Large Facultatively Sexual Populations , 2011, Genetics.

[45]  H. Ochman,et al.  Stepwise formation of the bacterial flagellar system , 2007, Proceedings of the National Academy of Sciences.

[46]  E. Ortlund,et al.  Crystal Structure of an Ancient Protein: Evolution by Conformational Epistasis , 2007, Science.

[47]  Stephen J Freeland,et al.  A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes , 2001, Genome Biology.

[48]  S. Teichmann,et al.  The importance of sequence diversity in the aggregation and evolution of proteins , 2005, Nature.

[49]  Ben Lehner,et al.  A simple principle concerning the robustness of protein complex activity to changes in gene expression , 2008 .

[50]  Jackson B. Lackey,et al.  Errata: Handbook of mathematical functions with formulas, graphs, and mathematical tables (Superintendent of Documents, U. S. Government Printing Office, Washington, D. C., 1964) by Milton Abramowitz and Irene A. Stegun , 1977 .

[51]  B. Chait,et al.  The molecular architecture of the nuclear pore complex , 2007, Nature.

[52]  Ariel Fernández,et al.  The nonconserved wrapping of conserved protein folds reveals a trend toward increasing connectivity in proteomic networks. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[53]  M. Lynch Scaling expectations for the time to establishment of complex adaptations , 2010, Proceedings of the National Academy of Sciences.

[54]  Michele Vendruscolo,et al.  Life on the edge: a link between gene expression levels and aggregation rates of human proteins. , 2007, Trends in biochemical sciences.

[55]  J. B. Walsh,et al.  Rate of Accumulation of Reproductive Isolation by Chromosome Rearrangements , 1982, The American Naturalist.

[56]  Z. Kelman,et al.  Structural and functional similarities of prokaryotic and eukaryotic DNA polymerase sliding clamps. , 1995, Nucleic acids research.

[57]  M. Nowak,et al.  Stochastic Tunnels in Evolutionary Dynamics , 2004, Genetics.

[58]  Thomas Madej,et al.  Functional states of homooligomers: insights from the evolution of glycosyltransferases. , 2010, Journal of molecular biology.

[59]  Andrés Moya,et al.  Genomic determinants of protein folding thermodynamics in prokaryotic organisms. , 2004, Journal of molecular biology.

[60]  Christine A Orengo,et al.  Comparative evolutionary analysis of protein complexes in E. coli and yeast , 2010, BMC Genomics.

[61]  Austin L. Hughes,et al.  Evolution of the proteasome components , 1997, Immunogenetics.

[62]  Hafumi Nishi,et al.  Caught in self-interaction: evolutionary and functional mechanisms of protein homooligomerization , 2011, Physical biology.

[63]  M. Lynch Rate, molecular spectrum, and consequences of human mutation , 2010, Proceedings of the National Academy of Sciences.

[64]  F. Hildebrand,et al.  Evidence of Selection upon Genomic GC-Content in Bacteria , 2010, PLoS genetics.

[65]  M. Lynch The Lower Bound to the Evolution of Mutation Rates , 2011, Genome biology and evolution.

[66]  Mot Kimuraz,et al.  ON THE PROBABILITY OF FIXATION OF MUTANT GENES IN A POPULATION’ , 2003 .

[67]  M. Matz,et al.  Retracing evolution of red fluorescence in GFP-like proteins from Faviina corals. , 2010, Molecular biology and evolution.

[68]  D. Eisenberg,et al.  Domain swapping: entangling alliances between proteins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Marcus W Feldman,et al.  The rate at which asexual populations cross fitness valleys. , 2009, Theoretical population biology.

[70]  M. Lynch,et al.  The rate of establishment of complex adaptations. , 2010, Molecular biology and evolution.

[71]  S. Teichmann,et al.  Assembly reflects evolution of protein complexes , 2008, Nature.

[72]  M. Lynch Evolution of the mutation rate. , 2010, Trends in genetics : TIG.

[73]  David Eisenberg,et al.  3D domain swapping: As domains continue to swap , 2002, Protein science : a publication of the Protein Society.

[74]  Huan Zhang,et al.  Elucidation of phenotypic adaptations: Molecular analyses of dim-light vision proteins in vertebrates , 2008, Proceedings of the National Academy of Sciences.

[75]  Gustavo Caetano-Anollés,et al.  Reductive evolution of proteomes and protein structures , 2011, Proceedings of the National Academy of Sciences.

[76]  Anirvan M. Sengupta,et al.  Mutation-selection networks of cancer initiation: tumor suppressor genes and chromosomal instability. , 2003, Journal of theoretical biology.

[77]  A. Bogan,et al.  Anatomy of hot spots in protein interfaces. , 1998, Journal of molecular biology.

[78]  J. Parker,et al.  Errors and alternatives in reading the universal genetic code. , 1989, Microbiological reviews.

[79]  Temple F. Smith,et al.  The origin and evolution of the ribosome , 2008, Biology Direct.

[80]  Ariel Fernández,et al.  Nonadaptive origins of interactome complexity , 2011, Nature.

[81]  E. Ortlund,et al.  Mechanisms for the Evolution of a Derived Function in the Ancestral Glucocorticoid Receptor , 2011, PLoS genetics.

[82]  Filipe Tavares-Cadete,et al.  Stepwise evolution of the centriole-assembly pathway , 2010, Journal of Cell Science.

[83]  A. Dean,et al.  Mechanistic approaches to the study of evolution: the functional synthesis , 2007, Nature Reviews Genetics.

[84]  I. Ispolatov,et al.  Binding properties and evolution of homodimers in protein–protein interaction networks , 2005, Nucleic acids research.