Upstream plasticity and downstream robustness in evolution of molecular networks

Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in living organisms. Recent species-wide data for protein-protein interactions and transcriptional regulations allow us to assess the effect of gene duplica...

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Published inBMC evolutionary biology Vol. 4; no. 1; p. 9
Main Authors Maslov, Sergei, Sneppen, Kim, Eriksen, Kasper Astrup, Yan, Koon-Kiu
Format Journal Article
LanguageEnglish
Published England BioMed Central Ltd 08.03.2004
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Abstract Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in living organisms. Recent species-wide data for protein-protein interactions and transcriptional regulations allow us to assess the effect of gene duplication on robustness and plasticity of these molecular networks. We demonstrate that the transcriptional regulation of duplicated genes in baker's yeast Saccharomyces cerevisiae diverges fast so that on average they lose 3% of common transcription factors for every 1% divergence of their amino acid sequences. The set of protein-protein interaction partners of their protein products changes at a slower rate exhibiting a broad plateau for amino acid sequence similarity above 70%. The stability of functional roles of duplicated genes at such relatively low sequence similarity is further corroborated by their ability to substitute for each other in single gene knockout experiments in yeast and RNAi experiments in a nematode worm Caenorhabditis elegans. We also quantified the divergence rate of physical interaction neighborhoods of paralogous proteins in a bacterium Helicobacter pylori and a fly Drosophila melanogaster. However, in the absence of system-wide data on transcription factors' binding in these organisms we could not compare this rate to that of transcriptional regulation of duplicated genes. For all molecular networks studied in this work we found that even the most distantly related paralogous proteins with amino acid sequence identities around 20% on average have more similar positions within a network than a randomly selected pair of proteins. For yeast we also found that the upstream regulation of genes evolves more rapidly than downstream functions of their protein products. This is in accordance with a view which puts regulatory changes as one of the main driving forces of the evolution. In this context a very important open question is to what extent our results obtained for homologous genes within a single species (paralogs) carries over to homologous proteins in different species (orthologs).
AbstractList Abstract Background Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in living organisms. Recent species-wide data for protein-protein interactions and transcriptional regulations allow us to assess the effect of gene duplication on robustness and plasticity of these molecular networks. Results We demonstrate that the transcriptional regulation of duplicated genes in baker's yeast Saccharomyces cerevisiae diverges fast so that on average they lose 3% of common transcription factors for every 1% divergence of their amino acid sequences. The set of protein-protein interaction partners of their protein products changes at a slower rate exhibiting a broad plateau for amino acid sequence similarity above 70%. The stability of functional roles of duplicated genes at such relatively low sequence similarity is further corroborated by their ability to substitute for each other in single gene knockout experiments in yeast and RNAi experiments in a nematode worm Caenorhabditis elegans. We also quantified the divergence rate of physical interaction neighborhoods of paralogous proteins in a bacterium Helicobacter pylori and a fly Drosophila melanogaster. However, in the absence of system-wide data on transcription factors' binding in these organisms we could not compare this rate to that of transcriptional regulation of duplicated genes. Conclusions For all molecular networks studied in this work we found that even the most distantly related paralogous proteins with amino acid sequence identities around 20% on average have more similar positions within a network than a randomly selected pair of proteins. For yeast we also found that the upstream regulation of genes evolves more rapidly than downstream functions of their protein products. This is in accordance with a view which puts regulatory changes as one of the main driving forces of the evolution. In this context a very important open question is to what extent our results obtained for homologous genes within a single species (paralogs) carries over to homologous proteins in different species (orthologs).
BACKGROUNDGene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in living organisms. Recent species-wide data for protein-protein interactions and transcriptional regulations allow us to assess the effect of gene duplication on robustness and plasticity of these molecular networks.RESULTSWe demonstrate that the transcriptional regulation of duplicated genes in baker's yeast Saccharomyces cerevisiae diverges fast so that on average they lose 3% of common transcription factors for every 1% divergence of their amino acid sequences. The set of protein-protein interaction partners of their protein products changes at a slower rate exhibiting a broad plateau for amino acid sequence similarity above 70%. The stability of functional roles of duplicated genes at such relatively low sequence similarity is further corroborated by their ability to substitute for each other in single gene knockout experiments in yeast and RNAi experiments in a nematode worm Caenorhabditis elegans. We also quantified the divergence rate of physical interaction neighborhoods of paralogous proteins in a bacterium Helicobacter pylori and a fly Drosophila melanogaster. However, in the absence of system-wide data on transcription factors' binding in these organisms we could not compare this rate to that of transcriptional regulation of duplicated genes.CONCLUSIONSFor all molecular networks studied in this work we found that even the most distantly related paralogous proteins with amino acid sequence identities around 20% on average have more similar positions within a network than a randomly selected pair of proteins. For yeast we also found that the upstream regulation of genes evolves more rapidly than downstream functions of their protein products. This is in accordance with a view which puts regulatory changes as one of the main driving forces of the evolution. In this context a very important open question is to what extent our results obtained for homologous genes within a single species (paralogs) carries over to homologous proteins in different species (orthologs).
Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in living organisms. Recent species-wide data for protein-protein interactions and transcriptional regulations allow us to assess the effect of gene duplication on robustness and plasticity of these molecular networks. We demonstrate that the transcriptional regulation of duplicated genes in baker's yeast Saccharomyces cerevisiae diverges fast so that on average they lose 3% of common transcription factors for every 1% divergence of their amino acid sequences. The set of protein-protein interaction partners of their protein products changes at a slower rate exhibiting a broad plateau for amino acid sequence similarity above 70%. The stability of functional roles of duplicated genes at such relatively low sequence similarity is further corroborated by their ability to substitute for each other in single gene knockout experiments in yeast and RNAi experiments in a nematode worm Caenorhabditis elegans. We also quantified the divergence rate of physical interaction neighborhoods of paralogous proteins in a bacterium Helicobacter pylori and a fly Drosophila melanogaster. However, in the absence of system-wide data on transcription factors' binding in these organisms we could not compare this rate to that of transcriptional regulation of duplicated genes. For all molecular networks studied in this work we found that even the most distantly related paralogous proteins with amino acid sequence identities around 20% on average have more similar positions within a network than a randomly selected pair of proteins. For yeast we also found that the upstream regulation of genes evolves more rapidly than downstream functions of their protein products. This is in accordance with a view which puts regulatory changes as one of the main driving forces of the evolution. In this context a very important open question is to what extent our results obtained for homologous genes within a single species (paralogs) carries over to homologous proteins in different species (orthologs).
BACKGROUND: Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in living organisms. Recent species-wide data for protein-protein interactions and transcriptional regulations allow us to assess the effect of gene duplication on robustness and plasticity of these molecular networks. RESULTS: We demonstrate that the transcriptional regulation of duplicated genes in baker's yeast Saccharomyces cerevisiae diverges fast so that on average they lose 3% of common transcription factors for every 1% divergence of their amino acid sequences. The set of protein-protein interaction partners of their protein products changes at a slower rate exhibiting a broad plateau for amino acid sequence similarity above 70%. The stability of functional roles of duplicated genes at such relatively low sequence similarity is further corroborated by their ability to substitute for each other in single gene knockout experiments in yeast and RNAi experiments in a nematode worm Caenorhabditis elegans. We also quantified the divergence rate of physical interaction neighborhoods of paralogous proteins in a bacterium Helicobacter pylori and a fly Drosophila melanogaster. However, in the absence of system-wide data on transcription factors' binding in these organisms we could not compare this rate to that of transcriptional regulation of duplicated genes. CONCLUSIONS: For all molecular networks studied in this work we found that even the most distantly related paralogous proteins with amino acid sequence identities around 20% on average have more similar positions within a network than a randomly selected pair of proteins. For yeast we also found that the upstream regulation of genes evolves more rapidly than downstream functions of their protein products. This is in accordance with a view which puts regulatory changes as one of the main driving forces of the evolution. In this context a very important open question is to what extent our results obtained for homologous genes within a single species (paralogs) carries over to homologous proteins in different species (orthologs).
Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in living organisms. Recent species-wide data for protein-protein interactions and transcriptional regulations allow us to assess the effect of gene duplication on robustness and plasticity of these molecular networks. We demonstrate that the transcriptional regulation of duplicated genes in baker's yeast Saccharomyces cerevisiae diverges fast so that on average they lose 3% of common transcription factors for every 1% divergence of their amino acid sequences. The set of protein-protein interaction partners of their protein products changes at a slower rate exhibiting a broad plateau for amino acid sequence similarity above 70%. The stability of functional roles of duplicated genes at such relatively low sequence similarity is further corroborated by their ability to substitute for each other in single gene knockout experiments in yeast and RNAi experiments in a nematode worm Caenorhabditis elegans. We also quantified the divergence rate of physical interaction neighborhoods of paralogous proteins in a bacterium Helicobacter pylori and a fly Drosophila melanogaster. However, in the absence of system-wide data on transcription factors' binding in these organisms we could not compare this rate to that of transcriptional regulation of duplicated genes. For all molecular networks studied in this work we found that even the most distantly related paralogous proteins with amino acid sequence identities around 20% on average have more similar positions within a network than a randomly selected pair of proteins. For yeast we also found that the upstream regulation of genes evolves more rapidly than downstream functions of their protein products. This is in accordance with a view which puts regulatory changes as one of the main driving forces of the evolution. In this context a very important open question is to what extent our results obtained for homologous genes within a single species (paralogs) carries over to homologous proteins in different species (orthologs).
ArticleNumber 9
Author Sneppen, Kim
Maslov, Sergei
Eriksen, Kasper Astrup
Yan, Koon-Kiu
AuthorAffiliation 2 Nordita, Blegdamsvej 17, 2100 Copenhagen Ø, Denmark
1 Department of Physics, Brookhaven National Laboratory, Upton, New York 11973, USA
4 Department of Physics and Astronomy, Stony Brook University, Stony Brook, New York 11794, USA
3 Department of Theoretical Physics, Lund University, Sölvegatan 14A, SE-223 62 Lund, Sweden
AuthorAffiliation_xml – name: 3 Department of Theoretical Physics, Lund University, Sölvegatan 14A, SE-223 62 Lund, Sweden
– name: 2 Nordita, Blegdamsvej 17, 2100 Copenhagen Ø, Denmark
– name: 4 Department of Physics and Astronomy, Stony Brook University, Stony Brook, New York 11794, USA
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  givenname: Sergei
  surname: Maslov
  fullname: Maslov, Sergei
  email: maslov@bnl.gov
  organization: Department of Physics, Brookhaven National Laboratory, Upton, New York 11973, USA. maslov@bnl.gov
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  surname: Eriksen
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  givenname: Koon-Kiu
  surname: Yan
  fullname: Yan, Koon-Kiu
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Cites_doi 10.1126/science.1090289
10.1016/S0022-2836(05)80360-2
10.1016/S0168-9525(03)00174-4
10.1093/oxfordjournals.molbev.a003913
10.1038/nature01198
10.1007/978-3-642-86659-3
10.1186/gb-2002-3-2-research0008
10.1038/nature00935
10.1073/pnas.061034498
10.1038/35001009
10.1126/science.1075090
10.1093/nar/30.1.145
10.1016/S0168-9525(02)02837-8
10.1038/ng929
10.1038/nature01278
10.1038/35051615
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References 12511954 - Nature. 2003 Jan 2;421(6918):63-6
2231712 - J Mol Biol. 1990 Oct 5;215(3):403-10
10688190 - Nature. 2000 Feb 10;403(6770):623-7
12399584 - Science. 2002 Oct 25;298(5594):799-804
11283351 - Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4569-74
11752277 - Nucleic Acids Res. 2002 Jan 1;30(1):145-8
12902158 - Trends Genet. 2003 Aug;19(8):417-22
11864370 - Genome Biol. 2002;3(2):RESEARCH0008
11420367 - Mol Biol Evol. 2001 Jul;18(7):1283-92
14605208 - Science. 2003 Dec 5;302(5651):1727-36
12140549 - Nature. 2002 Jul 25;418(6896):387-91
12529635 - Nature. 2003 Jan 16;421(6920):231-7
12134146 - Nat Genet. 2002 Aug;31(4):400-4
12446139 - Trends Genet. 2002 Dec;18(12):609-13
11196647 - Nature. 2001 Jan 11;409(6817):211-5
A Wagner (69_CR13) 2001; 18
FA Kondrashov (69_CR15) 2002; 3
B Papp (69_CR12) 2003; 19
DG Gilbert (69_CR18) 2002; 30
P Uetz (69_CR3) 2000; 403
Z Gu (69_CR11) 2002; 18
S Ohno (69_CR1) 1970
RS Kamath (69_CR8) 2003; 421
LM Steinmetz (69_CR10) 2002; 31
SF Altschul (69_CR9) 1990; 215
TI Lee (69_CR2) 2002; 298
T Ito (69_CR4) 2001; 98
L Giot (69_CR7) 2003; 302
Z Gu (69_CR14) 2003; 421
JC Rain (69_CR6) 2001; 409
G Giaever (69_CR5) 2002; 418
69_CR17
69_CR16
References_xml – volume: 302
  start-page: 1727
  year: 2003
  ident: 69_CR7
  publication-title: Science
  doi: 10.1126/science.1090289
  contributor:
    fullname: L Giot
– volume: 215
  start-page: 403
  year: 1990
  ident: 69_CR9
  publication-title: J Mol Biol
  doi: 10.1016/S0022-2836(05)80360-2
  contributor:
    fullname: SF Altschul
– volume: 19
  start-page: 417
  year: 2003
  ident: 69_CR12
  publication-title: Trends in Genetics
  doi: 10.1016/S0168-9525(03)00174-4
  contributor:
    fullname: B Papp
– volume: 18
  start-page: 1283
  year: 2001
  ident: 69_CR13
  publication-title: Mol Biol Evol
  doi: 10.1093/oxfordjournals.molbev.a003913
  contributor:
    fullname: A Wagner
– volume: 421
  start-page: 63
  year: 2003
  ident: 69_CR14
  publication-title: Nature
  doi: 10.1038/nature01198
  contributor:
    fullname: Z Gu
– volume-title: Evolution by gene duplication
  year: 1970
  ident: 69_CR1
  doi: 10.1007/978-3-642-86659-3
  contributor:
    fullname: S Ohno
– volume: 3
  start-page: RESEARCH0008.10
  issue: 2
  year: 2002
  ident: 69_CR15
  publication-title: Genome Biology
  doi: 10.1186/gb-2002-3-2-research0008
  contributor:
    fullname: FA Kondrashov
– volume: 418
  start-page: 387
  year: 2002
  ident: 69_CR5
  publication-title: Nature
  doi: 10.1038/nature00935
  contributor:
    fullname: G Giaever
– volume: 98
  start-page: 4569
  year: 2001
  ident: 69_CR4
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.061034498
  contributor:
    fullname: T Ito
– ident: 69_CR17
– ident: 69_CR16
– volume: 403
  start-page: 623
  year: 2000
  ident: 69_CR3
  publication-title: Nature
  doi: 10.1038/35001009
  contributor:
    fullname: P Uetz
– volume: 298
  start-page: 799
  year: 2002
  ident: 69_CR2
  publication-title: Science
  doi: 10.1126/science.1075090
  contributor:
    fullname: TI Lee
– volume: 30
  start-page: 145
  year: 2002
  ident: 69_CR18
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/30.1.145
  contributor:
    fullname: DG Gilbert
– volume: 18
  start-page: 609
  year: 2002
  ident: 69_CR11
  publication-title: Trends in Genetics
  doi: 10.1016/S0168-9525(02)02837-8
  contributor:
    fullname: Z Gu
– volume: 31
  start-page: 400
  year: 2002
  ident: 69_CR10
  publication-title: Nature Genetics
  doi: 10.1038/ng929
  contributor:
    fullname: LM Steinmetz
– volume: 421
  start-page: 231
  year: 2003
  ident: 69_CR8
  publication-title: Nature
  doi: 10.1038/nature01278
  contributor:
    fullname: RS Kamath
– volume: 409
  start-page: 211
  year: 2001
  ident: 69_CR6
  publication-title: Nature
  doi: 10.1038/35051615
  contributor:
    fullname: JC Rain
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Snippet Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in living...
BACKGROUNDGene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in...
BACKGROUND: Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in...
Background: Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular networks in...
Abstract Background Gene duplication followed by the functional divergence of the resulting pair of paralogous proteins is a major force shaping molecular...
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SubjectTerms Animals
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biofysiks
Biologi
Biological Sciences
Biophysics
Caenorhabditis elegans
Caenorhabditis elegans - genetics
Drosophila melanogaster
Drosophila melanogaster - genetics
Evolution, Molecular
Fungal Proteins - genetics
Fungal Proteins - metabolism
Gene Duplication
Gene Expression Regulation
Genes, Duplicate - genetics
Genetic Variation
Helicobacter pylori
Helicobacter pylori - genetics
Helminth Proteins - genetics
Helminth Proteins - metabolism
Insect Proteins - genetics
Insect Proteins - metabolism
Natural Sciences
Naturvetenskap
Nematoda
Protein Binding
RNA Interference
Saccharomyces cerevisiae
Saccharomyces cerevisiae - genetics
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Title Upstream plasticity and downstream robustness in evolution of molecular networks
URI https://www.ncbi.nlm.nih.gov/pubmed/15070432
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http://dx.doi.org/10.1186/1471-2148-4-9
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https://lup.lub.lu.se/record/283039
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