Home LiteratureArticle Details
PMID: 12952876 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Asymmetric sequence divergence of duplicate genes.

Genome research ·Vol. 13 ·No. 9 ·2003-09-00 ·Pages 2052-8

Conant GC, Wagner A

Abstract

Much like humans, gene duplicates may be created equal, but they do not stay that way for long. For four completely sequenced genomes we show that 20%-30% of duplicate gene pairs show asymmetric evolution in the amino acid sequence of their protein products. That is, one of the duplicates evolves much faster than the other. The greater this asymmetry, the greater the ratio Ka/Ks of amino acid substitutions (Ka) to silent substitutions (Ks) in a gene pair. This indicates that most asymmetric divergence may be caused by relaxed selective constraints on one of the duplicates. However, we also find some candidate duplicates where positive (directional) selection of beneficial mutations (Ka/Ks > 1) may play a role in asymmetric divergence. Our analysis rests on a codon-based model of molecular evolution that allows a test for asymmetric divergence in Ka. The method is also more sensitive in detecting positive selection (Ka/Ks > 1) than models relying only on pairwise gene comparisons.

MeSH Terms
Amino Acid Substitution/genetics Animals Caenorhabditis elegans/genetics Computational Biology/methods,statistics & numerical data Drosophila melanogaster/genetics Evolution, Molecular Gene Expression Profiling/methods,statistics & numerical data Gene Expression Regulation/genetics Gene Expression Regulation, Fungal/genetics Genes, Duplicate Genetic Variation/genetics Saccharomyces cerevisiae/genetics Schizosaccharomyces/genetics
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Conant Gavin C
Department of Biology, The University of New Mexico, Albuquerque, New Mexico 87131, USA. gconant@unm.edu
Wagner Andreas
References (58)
58 references, click to expand
  1. Preservation of duplicate genes by complementary, degenerative mutations.
    Genetics. 1999 Apr;151(4):1531-45 PMID: 10101175
  2. Statistical tests of models of DNA substitution.
    J Mol Evol. 1993 Feb;36(2):182-98 PMID: 7679448
  3. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization.
    Mol Biol Cell. 1998 Dec;9(12):3273-97 PMID: 9843569
  4. A systematic gene expression screen of Caenorhabditis elegans cytochrome P450 genes reveals CYP35 as strongly xenobiotic inducible.
    Arch Biochem Biophys. 2001 Nov 15;395(2):158-68 PMID: 11697852
  5. A gene expression map for Caenorhabditis elegans.
    Science. 2001 Sep 14;293(5537):2087-92 PMID: 11557892
  6. Positive Darwinian selection after gene duplication in primate ribonuclease genes.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3708-13 PMID: 9520431
  7. The lysozyme locus in Drosophila melanogaster: an expanded gene family adapted for expression in the digestive tract.
    Mol Gen Genet. 1994 Jan;242(2):152-62 PMID: 8159165
  8. Gene duplication: past, present and future.
    Semin Cell Dev Biol. 1999 Oct;10(5):541-7 PMID: 10597638
  9. Life with 6000 genes.
    Science. 1996 Oct 25;274(5287):546, 563-7 PMID: 8849441
  10. Phylogenetic systematics turns over a new leaf.
    Trends Ecol Evol. 2001 Jan 1;16(1):30-37 PMID: 11146142
  11. Asymmetric functional divergence of duplicate genes in yeast.
    Mol Biol Evol. 2002 Oct;19(10):1760-8 PMID: 12270902
  12. Rate of gene silencing at duplicate loci: a theoretical study and interpretation of data from tetraploid fishes.
    Genetics. 1980 May;95(1):237-58 PMID: 7429144
  13. Testing the neutral theory of molecular evolution with genomic data from Drosophila.
    Nature. 2002 Feb 28;415(6875):1024-6 PMID: 11875569
  14. Adaptive protein evolution in Drosophila.
    Nature. 2002 Feb 28;415(6875):1022-4 PMID: 11875568
  15. A comprehensive two-hybrid analysis to explore the yeast protein interactome.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4569-74 PMID: 11283351
  16. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome.
    Mol Biol Evol. 1994 Sep;11(5):715-24 PMID: 7968485
  17. A codon-based model of nucleotide substitution for protein-coding DNA sequences.
    Mol Biol Evol. 1994 Sep;11(5):725-36 PMID: 7968486
  18. Functional discovery via a compendium of expression profiles.
    Cell. 2000 Jul 7;102(1):109-26 PMID: 10929718
  19. The F-box protein family.
    Genome Biol. 2000;1(5):REVIEWS3002 PMID: 11178263
  20. Decoupled evolution of coding region and mRNA expression patterns after gene duplication: implications for the neutralist-selectionist debate.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6579-84 PMID: 10823904
  21. Evolution of duplicate genes in a tetraploid animal, Xenopus laevis.
    Mol Biol Evol. 1993 Nov;10(6):1360-9 PMID: 8277859
  22. Genome sequence of the nematode C. elegans: a platform for investigating biology.
    Science. 1998 Dec 11;282(5396):2012-8 PMID: 9851916
  23. Evolutionary preservation of redundant duplicated genes.
    Semin Cell Dev Biol. 1999 Oct;10(5):555-9 PMID: 10597640
  24. Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1598-603 PMID: 11818544
  25. Molecular adaptation of Drosophila melanogaster lysozymes to a digestive function.
    Insect Biochem Mol Biol. 1998 May-Jun;28(5-6):309-19 PMID: 9692234
  26. A variant beta-tubulin isoform of Drosophila melanogaster (beta 3) is expressed primarily in tissues of mesodermal origin in embryos and pupae, and is utilized in populations of transient microtubules.
    Dev Biol. 1989 Feb;131(2):415-29 PMID: 2492243
  27. Rapid evolution of male reproductive genes in the descent of man.
    Nature. 2000 Jan 20;403(6767):304-9 PMID: 10659848
  28. Selective sweep of a newly evolved sperm-specific gene in Drosophila.
    Nature. 1998 Dec 10;396(6711):572-5 PMID: 9859991
  29. Yeast genome duplication was followed by asynchronous differentiation of duplicated genes.
    Nature. 2003 Feb 20;421(6925):848-52 PMID: 12594514
  30. Genomic expression programs in the response of yeast cells to environmental changes.
    Mol Biol Cell. 2000 Dec;11(12):4241-57 PMID: 11102521
  31. Phylogenetic analysis of vertebrate lactate dehydrogenase (LDH) multigene families.
    J Mol Evol. 2002 May;54(5):614-24 PMID: 11965434
  32. Differential selection after duplication in mammalian developmental genes.
    Mol Biol Evol. 2001 Apr;18(4):557-62 PMID: 11264407
  33. Genetic redundancy in vertebrates: polyploidy and persistence of genes encoding multidomain proteins.
    Trends Genet. 1998 Feb;14(2):46-9; discussion 49-50 PMID: 9520595
  34. Tissue-specific microtubule functions in Drosophila spermatogenesis require the beta 2-tubulin isotype-specific carboxy terminus.
    Dev Biol. 1993 Jul;158(1):213-27 PMID: 8330671
  35. The ghost of selection past: rates of evolution and functional divergence of anciently duplicated genes.
    J Mol Evol. 2001 Oct-Nov;53(4-5):436-46 PMID: 11675603
  36. Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli.
    Nature. 2002 Oct 31;419(6910):899-903 PMID: 12410303
  37. Testing for equality of evolutionary rates.
    Genetics. 1992 Sep;132(1):269-76 PMID: 1398060
  38. GenomeHistory: a software tool and its application to fully sequenced genomes.
    Nucleic Acids Res. 2002 Aug 1;30(15):3378-86 PMID: 12140322
  39. Codon selection in yeast.
    J Biol Chem. 1982 Mar 25;257(6):3026-31 PMID: 7037777
  40. Microevolutionary studies in nematodes: a beginning.
    Bioessays. 2001 Sep;23(9):807-19 PMID: 11536293
  41. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae.
    Nature. 2000 Feb 10;403(6770):623-7 PMID: 10688190
  42. Structural analysis of mutations in the Drosophila beta 2-tubulin isoform reveals regions in the beta-tubulin molecular required for general and for tissue-specific microtubule functions.
    Genetics. 1995 Jan;139(1):267-86 PMID: 7705629
  43. Subcellular localization of the yeast proteome.
    Genes Dev. 2002 Mar 15;16(6):707-19 PMID: 11914276
  44. Primary structure requirements for correct sorting of the yeast mitochondrial protein ADH III to the yeast mitochondrial matrix space.
    Mol Cell Biol. 1987 Jan;7(1):294-304 PMID: 3550419
  45. Selection in the evolution of gene duplications.
    Genome Biol. 2002;3(2):RESEARCH0008 PMID: 11864370
  46. The genome sequence of Schizosaccharomyces pombe.
    Nature. 2002 Feb 21;415(6874):871-80 PMID: 11859360
  47. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
  48. Two Drosophila beta tubulin isoforms are not functionally equivalent.
    J Cell Biol. 1990 Sep;111(3):1009-26 PMID: 2118141
  49. The lysozyme locus in Drosophila melanogaster: different genes are expressed in midgut and salivary glands.
    Mol Gen Genet. 1992 Apr;232(3):335-43 PMID: 1588905
  50. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  51. SGD: Saccharomyces Genome Database.
    Nucleic Acids Res. 1998 Jan 1;26(1):73-9 PMID: 9399804
  52. Evolutionary trees from DNA sequences: a maximum likelihood approach.
    J Mol Evol. 1981;17(6):368-76 PMID: 7288891
  53. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism.
    Mol Biol Evol. 1998 Aug;15(8):1040-6 PMID: 9718731
  54. WormBase: network access to the genome and biology of Caenorhabditis elegans.
    Nucleic Acids Res. 2001 Jan 1;29(1):82-6 PMID: 11125056
  55. Adaptive diversification within a large family of recently duplicated, placentally expressed genes.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3319-23 PMID: 10725351
  56. The FlyBase database of the Drosophila genome projects and community literature.
    Nucleic Acids Res. 2002 Jan 1;30(1):106-8 PMID: 11752267
  57. Models of molecular evolution and phylogeny.
    Genome Res. 1998 Dec;8(12):1233-44 PMID: 9872979
  58. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi.
    Nature. 2003 Jan 16;421(6920):231-7 PMID: 12529635
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
DOI
10.1101/gr.1252603
Email
gconant@unm.edu
Published
2003-09-00
Pages
2052-8
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC403682
Subset
IM
Grants
NIGMS NIH HHS · R01 GM063882 · United States
NIGMS NIH HHS · GM063882-01 · United States
External Links
PubMed source DOI: 10.1101/gr.1252603 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2