Relative predicted protein levels of functionally associated proteins are conserved across organisms

We show that the predicted protein levels of functionally related proteins change in a coordinated fashion over many unicellular organisms. For each protein, we created a profile containing a protein abundance measure in each of a set of organisms. We show that for functionally related proteins these profiles tend to be correlated. Using the Codon Adaptation Index as a predictor of protein abundance in 48 unicellular organisms, we demonstrated this phenomenon for two types of functional relations: for proteins that physically interact and for proteins involved in consecutive steps within a metabolic pathway. Our results suggest that the protein abundance levels of functionally related proteins co-evolve.

[1]  P. Sharp,et al.  Codon usage and base composition inRickettsia prowazekii , 1996, Journal of Molecular Evolution.

[2]  E. Koonin,et al.  Evolution of bacterial RNA polymerase: implications for large-scale bacterial phylogeny, domain accretion, and horizontal gene transfer. , 2004, Gene.

[3]  A. E. Hirsh,et al.  Coevolution of gene expression among interacting proteins , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Folker Meyer,et al.  Comparing expression level‐dependent features in codon usage with protein abundance: An analysis of ‘predictive proteomics’ , 2004, Proteomics.

[5]  H. Margalit,et al.  Hierarchy of sequence-dependent features associated with prokaryotic translation. , 2003, Genome research.

[6]  E. O’Shea,et al.  Global analysis of protein expression in yeast , 2003, Nature.

[7]  S. Rhee,et al.  AraCyc: A Biochemical Pathway Database for Arabidopsis1 , 2003, Plant Physiology.

[8]  M. Smolka,et al.  Proteome analysis of the plant pathogen Xylella fastidiosa reveals major cellular and extracellular proteins and a peculiar codon bias distribution , 2003, Proteomics.

[9]  G. Perrière,et al.  Use and misuse of correspondence analysis in codon usage studies. , 2002, Nucleic acids research.

[10]  Peter D. Karp,et al.  The Pathway Tools software , 2002, ISMB.

[11]  Hidemasa Bono,et al.  Functional transcriptomes: comparative analysis of biological pathways and processes in eukaryotes to infer genetic networks among transcripts. , 2002, Current opinion in structural biology.

[12]  S. Verjovski-Almeida,et al.  Whole-Genome Analysis of Transporters in the Plant Pathogen Xylella fastidiosa , 2002, Microbiology and Molecular Biology Reviews.

[13]  P. Kemmeren,et al.  Protein interaction verification and functional annotation by integrated analysis of genome-scale data. , 2002, Molecular cell.

[14]  Charles DeLisi,et al.  Identifying functional links between genes using conserved chromosomal proximity. , 2002, Trends in genetics : TIG.

[15]  Ioannis Xenarios,et al.  DIP, the Database of Interacting Proteins: a research tool for studying cellular networks of protein interactions , 2002, Nucleic Acids Res..

[16]  M. Gerstein,et al.  Relating whole-genome expression data with protein-protein interactions. , 2002, Genome research.

[17]  Shigehiko Kanaya,et al.  Codon Usage and tRNA Genes in Eukaryotes: Correlation of Codon Usage Diversity with Translation Efficiency and with CG-Dinucleotide Usage as Assessed by Multivariate Analysis , 2001, Journal of Molecular Evolution.

[18]  M. Ermolaeva,et al.  Synonymous codon usage in bacteria. , 2001, Current issues in molecular biology.

[19]  Masasuke Yoshida,et al.  ATP synthase — a marvellous rotary engine of the cell , 2001, Nature Reviews Molecular Cell Biology.

[20]  A. Grigoriev.  A relationship between gene expression and protein interactions on the proteome scale: analysis of the bacteriophage T7 and the yeast Saccharomyces cerevisiae. , 2001, Nucleic acids research.

[21]  S. Karlin,et al.  Characterizations of Highly Expressed Genes of Four Fast-Growing Bacteria , 2001, Journal of bacteriology.

[22]  Michael Y. Galperin,et al.  The COG database: new developments in phylogenetic classification of proteins from complete genomes , 2001, Nucleic Acids Res..

[23]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[24]  P. Sharp,et al.  Absence of translationally selected synonymous codon usage bias in Helicobacter pylori. , 2000, Microbiology.

[25]  Anton J. Enright,et al.  Protein interaction maps for complete genomes based on gene fusion events , 1999, Nature.

[26]  S. Kanaya,et al.  Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. , 1999, Gene.

[27]  D. Eisenberg,et al.  Detecting protein function and protein-protein interactions from genome sequences. , 1999, Science.

[28]  D. Eisenberg,et al.  Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Overbeek,et al.  The use of gene clusters to infer functional coupling. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[30]  B. Snel,et al.  Conservation of gene order: a fingerprint of proteins that physically interact. , 1998, Trends in biochemical sciences.

[31]  S Karlin,et al.  Codon usages in different gene classes of the Escherichia coli genome , 1998, Molecular microbiology.

[32]  P. Bork,et al.  Measuring genome evolution. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  K. Severinov,et al.  Tethering of the Large Subunits of Escherichia coli RNA Polymerase* , 1997, The Journal of Biological Chemistry.

[34]  P. Boyer.  The ATP synthase--a splendid molecular machine. , 1997, Annual review of biochemistry.

[35]  George M. Church,et al.  Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K‐12 , 1997, Electrophoresis.

[36]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[37]  C. Kurland,et al.  Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. , 1996, Journal of molecular biology.

[38]  P. Lio’,et al.  Histidine biosynthetic pathway and genes: structure, regulation, and evolution. , 1996, Microbiological reviews.

[39]  D. Drapier,et al.  Evidence for Nuclear Control of the Expression of the atpA and atpB Chloroplast Genes in Chlamydomonas. , 1992, The Plant cell.

[40]  F. Wright.  The 'effective number of codons' used in a gene. , 1990, Gene.

[41]  P. Sharp,et al.  The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. , 1987, Nucleic acids research.

[42]  T. Ikemura.  Codon usage and tRNA content in unicellular and multicellular organisms. , 1985, Molecular biology and evolution.

[43]  T. Ikemura.  Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes. Differences in synonymous codon choice patterns of yeast and Escherichia coli with reference to the abundance of isoaccepting transfer RNAs. , 1982, Journal of molecular biology.

[44]  T. Ikemura.  Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. , 1981, Journal of molecular biology.