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PMID: 17726166 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A model of segmental duplication formation in Drosophila melanogaster.

Genome research ·Vol. 17 ·No. 10 ·2007-10-00 ·Pages 1458-70

Fiston-Lavier AS, Anxolabehere D, Quesneville H

Abstract

Segmental duplications (SDs) are low-copy repeats of DNA segments that have long been recognized to be involved in genome organization and evolution. But, to date, the mechanism of their formation remains obscure. We propose a model for SD formation that we name "duplication-dependent strand annealing" (DDSA). This model is a variant of the synthesis-dependent strand annealing (SDSA) model--a double-strand break (DSB) homologous repair model. DSB repair in Drosophila melanogaster genome usually occurs primarily through homologous repair, more preferentially through the SDSA model. The DDSA model predicts that after a DSB, the search for an ectopic homologous region--here a repeat--initiates the repair. As expected by the model, the analysis of SDs detected by a computational analysis of the D. melanogaster genome indicates a high enrichment in transposable elements at SD ends. It shows moreover a preferential location of SDs in heterochromatic regions. The model has the advantage of also predicting specific traces left during synthesis. The observed traces support the DDSA model as one model of formation of SDs in D. melanogaster genome. The analysis of these DDSA signatures suggests moreover a sequestration of the dissociated strand in the repair complex.

MeSH Terms
Animals Base Sequence DNA/genetics DNA Breaks, Double-Stranded DNA Repair/genetics Drosophila melanogaster/genetics,metabolism Gene Duplication Genes, Insect Genome, Insect Heterochromatin/genetics Models, Genetic Molecular Sequence Data Repetitive Sequences, Nucleic Acid Sequence Homology, Nucleic Acid Tandem Repeat Sequences
Chemicals
Heterochromatin DNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Fiston-Lavier Anna-Sophie
Laboratoire Bioinformatique et Génomique, Institut Jacques Monod, 75005 Paris, France.
Anxolabehere Dominique
Quesneville Hadi
References (59)
59 references, click to expand
  1. Purification and characterization of the T4 bacteriophage uvsX protein.
    J Biol Chem. 1986 May 5;261(13):6107-18 PMID: 2939071
  2. It takes two transposons to tango: transposable-element-mediated chromosomal rearrangements.
    Trends Genet. 2000 Oct;16(10):461-8 PMID: 11050333
  3. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 1999 Jun;63(2):349-404 PMID: 10357855
  4. Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster.
    Genetics. 1993 Aug;134(4):1149-74 PMID: 8375654
  5. Reptitive DNA sequences in drosophila.
    Chromosoma. 1971;33(3):319-44 PMID: 5088497
  6. Eukaryotic transposable elements and genome evolution.
    Trends Genet. 1989 Apr;5(4):103-7 PMID: 2543105
  7. Gene duplications and the origins of vertebrate development.
    Dev Suppl. 1994;:125-33 PMID: 7579513
  8. Genomic disorders: structural features of the genome can lead to DNA rearrangements and human disease traits.
    Trends Genet. 1998 Oct;14(10):417-22 PMID: 9820031
  9. Recent segmental duplications in the human genome.
    Science. 2002 Aug 9;297(5583):1003-7 PMID: 12169732
  10. Patterns of insertion and deletion in contrasting chromatin domains.
    Mol Biol Evol. 2002 Dec;19(12):2211-25 PMID: 12446812
  11. Segmental duplications and the evolution of the primate genome.
    Nat Rev Genet. 2002 Jan;3(1):65-72 PMID: 11823792
  12. Repbase update: a database and an electronic journal of repetitive elements.
    Trends Genet. 2000 Sep;16(9):418-20 PMID: 10973072
  13. Detection of new transposable element families in Drosophila melanogaster and Anopheles gambiae genomes.
    J Mol Evol. 2003;57 Suppl 1:S50-9 PMID: 15008403
  14. Structure, molecular evolution and maintenance of copy number of extended repeated structures in the X-heterochromatin of Drosophila melanogaster.
    Chromosoma. 1994 Jul;103(4):277-85 PMID: 7988289
  15. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations.
    Genes Dev. 1998 Dec 15;12(24):3831-42 PMID: 9869637
  16. Tandem repeats finder: a program to analyze DNA sequences.
    Nucleic Acids Res. 1999 Jan 15;27(2):573-80 PMID: 9862982
  17. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data.
    Mol Biol Evol. 1997 Jul;14(7):685-95 PMID: 9254330
  18. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.
    J Mol Evol. 1985;22(2):160-74 PMID: 3934395
  19. Distribution of Induced Breaks along the X-Chromosome of Drosophila Melanogaster.
    Proc Natl Acad Sci U S A. 1939 Nov;25(11):571-7 PMID: 16577949
  20. Molecular-evolutionary mechanisms for genomic disorders.
    Curr Opin Genet Dev. 2002 Jun;12(3):312-9 PMID: 12076675
  21. Combined evidence annotation of transposable elements in genome sequences.
    PLoS Comput Biol. 2005 Jul;1(2):166-75 PMID: 16110336
  22. Segmental duplications: organization and impact within the current human genome project assembly.
    Genome Res. 2001 Jun;11(6):1005-17 PMID: 11381028
  23. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster.
    Bioessays. 1994 Apr;16(4):269-75 PMID: 8031304
  24. Eukaryote genome duplication - where's the evidence?
    Curr Opin Genet Dev. 1998 Dec;8(6):694-700 PMID: 9914206
  25. Heterochromatic sequences in a Drosophila whole-genome shotgun assembly.
    Genome Biol. 2002;3(12):RESEARCH0085 PMID: 12537574
  26. Concerted and birth-and-death evolution of multigene families.
    Annu Rev Genet. 2005;39:121-52 PMID: 16285855
  27. Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments.
    EMBO J. 2004 Jan 14;23(1):234-43 PMID: 14685272
  28. The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila.
    Genetics. 2003 Dec;165(4):1831-42 PMID: 14704169
  29. Cloning and characterization of a dispersed, multicopy, X chromosome sequence in Drosophila melanogaster.
    Proc Natl Acad Sci U S A. 1987 May;84(9):2843-7 PMID: 3106978
  30. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  31. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.
    Syst Biol. 2003 Oct;52(5):696-704 PMID: 14530136
  32. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair.
    Mol Cell Biol. 1994 Mar;14(3):1613-25 PMID: 8114699
  33. On the rate of DNA sequence evolution in Drosophila.
    J Mol Evol. 1989 May;28(5):398-402 PMID: 2501501
  34. Initial sequencing and comparative analysis of the mouse genome.
    Nature. 2002 Dec 5;420(6915):520-62 PMID: 12466850
  35. Complex evolution of 7E olfactory receptor genes in segmental duplications.
    Genome Res. 2003 May;13(5):781-93 PMID: 12727898
  36. Mini- and microsatellite expansions: the recombination connection.
    EMBO Rep. 2000 Aug;1(2):122-6 PMID: 11265750
  37. High-frequency P element loss in Drosophila is homolog dependent.
    Cell. 1990 Aug 10;62(3):515-25 PMID: 2165865
  38. Gene and genome duplication.
    Curr Opin Genet Dev. 2001 Dec;11(6):681-4 PMID: 11682313
  39. An Alu transposition model for the origin and expansion of human segmental duplications.
    Am J Hum Genet. 2003 Oct;73(4):823-34 PMID: 14505274
  40. Copies of a Stellate gene variant are located in the X heterochromatin of Drosophila melanogaster and are probably expressed.
    Genetics. 1992 Dec;132(4):1033-7 PMID: 1459425
  41. Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome.
    Genome Biol. 2006;7(11):R112 PMID: 17134480
  42. Evidence for multiple cycles of strand invasion during repair of double-strand gaps in Drosophila.
    Genetics. 2004 Jun;167(2):699-705 PMID: 15238522
  43. The double-strand-break repair model for recombination.
    Cell. 1983 May;33(1):25-35 PMID: 6380756
  44. The sequencing of the rat genome.
    Eur J Surg Oncol. 2004 Oct;30(8):905-6 PMID: 15497215
  45. The sequence of the human genome.
    Science. 2001 Feb 16;291(5507):1304-51 PMID: 11181995
  46. BAR DUPLICATION.
    Science. 1936 May 29;83(2161):528-30 PMID: 17806465
  47. Heterochromatic Stellate gene cluster in Drosophila melanogaster: structure and molecular evolution.
    Genetics. 1997 May;146(1):253-62 PMID: 9136015
  48. Charcot-Marie-Tooth disease: lessons in genetic mechanisms.
    Mol Med. 1998 Jan;4(1):3-11 PMID: 9513184
  49. Eu-heterochromatic rearrangements induce replication of heterochromatic sequences normally underreplicated in polytene chromosomes of Drosophila melanogaster.
    Genetics. 2005 Dec;171(4):1673-81 PMID: 16020783
  50. Segmental duplications: what's missing, misassigned, and misassembled--and should we care?
    Genome Res. 2001 May;11(5):653-6 PMID: 11337463
  51. Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication.
    Nature. 2005 Sep 1;437(7055):94-100 PMID: 16136133
  52. 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
  53. Recent segmental and gene duplications in the mouse genome.
    Genome Biol. 2003;4(8):R47 PMID: 12914656
  54. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination.
    Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9214-9 PMID: 9256462
  55. The fourth chromosome of Drosophila melanogaster: interspersed euchromatic and heterochromatic domains.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5340-5 PMID: 10779561
  56. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  57. 2002 Curt Stern Award Address. Genomic disorders recombination-based disease resulting from genomic architecture.
    Am J Hum Genet. 2003 Feb;72(2):246-52 PMID: 12596790
  58. Initial sequencing and analysis of the human genome.
    Nature. 2001 Feb 15;409(6822):860-921 PMID: 11237011
  59. Gen(om)e duplications in the evolution of early vertebrates.
    Curr Opin Genet Dev. 1996 Dec;6(6):715-22 PMID: 8994842
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
DOI
10.1101/gr.6208307
Published
2007-10-00
Epub
2007-00-28
Pages
1458-70
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC1987339
Subset
IM
External Links
PubMed source DOI: 10.1101/gr.6208307 PMC Full Text View journal details
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