Home LiteratureArticle Details
PMID: 11157786 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila.

Genome research ·Vol. 11 ·No. 2 ·2001-02-00 ·Pages 230-9

Ranz JM, Casals F, Ruiz A

Abstract

During the evolution of the genus Drosophila, the molecular organization of the major chromosomal elements has been repeatedly rearranged via the fixation of paracentric inversions. Little detailed information is available, however, on the extent and effect of these changes at the molecular level. In principle, a full description of the rate and pattern of change could reveal the limits, if any, to which the eukaryotic genome can accommodate reorganizations. We have constructed a high-density physical map of the largest chromosomal element in Drosophila repleta (chromosome 2) and compared the order and distances between the markers with those on the homologous chromosomal element (3R) in Drosophila melanogaster. The two species belong to different subgenera (Drosophila and Sophophora, respectively), which diverged 40-62 million years (Myr) ago and represent, thus, the farthest lineages within the Drosophila genus. The comparison reveals extensive reshuffling of gene order from centromere to telomere. Using a maximum likelihood method, we estimate that 114 +/- 14 paracentric inversions have been fixed in this chromosomal element since the divergence of the two species, that is, 0.9-1.4 inversions fixed per Myr. Comparison with available rates of chromosomal evolution, taking into account genome size, indicates that the Drosophila genome shows the highest rate found so far in any eukaryote. Twenty-one small segments (23-599 kb) comprising at least two independent (nonoverlapping) markers appear to be conserved between D. melanogaster and D. repleta. These results are consistent with the random breakage model and do not provide significant evidence of functional constraint of any kind. They support the notion that the Drosophila genome is extraordinarily malleable and has a modular organization. The high rate of chromosomal change also suggests a very limited transferability of the positional information from the Drosophila genome to other insects.

MeSH Terms
Animals Base Composition Chromosome Inversion Chromosome Mapping Conserved Sequence Drosophila/genetics Drosophila melanogaster/genetics Eukaryotic Cells/chemistry,physiology Evolution, Molecular Gene Order Gene Rearrangement Genes, Insect/genetics Genetic Markers Genome Molecular Sequence Data
Chemicals
Genetic Markers
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ranz J M
Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain. jranz@oeb.harvard.edu
Casals F
Ruiz A
References (58)
58 references, click to expand
  1. Comparative mapping of cosmids and gene clones from a 1.6 Mb chromosomal region of Drosophila melanogaster in three species of the distantly related subgenus Drosophila.
    Chromosoma. 1999 Apr;108(1):32-43 PMID: 10199954
  2. Genome mapping in capsicum and the evolution of genome structure in the solanaceae.
    Genetics. 1999 Jul;152(3):1183-202 PMID: 10388833
  3. Construction and characterization of bacterial artificial chromosome libraries from the silkworm, Bombyx mori.
    Mol Gen Genet. 1999 Jun;261(4-5):698-706 PMID: 10394907
  4. Generation of a widespread Drosophila inversion by a transposable element.
    Science. 1999 Jul 16;285(5426):415-8 PMID: 10411506
  5. stress sensitive B encodes an adenine nucleotide translocase in Drosophila melanogaster.
    Genetics. 1999 Oct;153(2):891-903 PMID: 10511565
  6. The promise of comparative genomics in mammals.
    Science. 1999 Oct 15;286(5439):458-62, 479-81 PMID: 10521336
  7. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
  8. Comparative genome mapping in the sequence-based era: early experience with human chromosome 7.
    Genome Res. 2000 May;10(5):624-33 PMID: 10810084
  9. Molecular organization of the Drosophila melanogaster Adh chromosomal region in D. repleta and D. buzzatii, two distantly related species of the Drosophila subgenus.
    Chromosome Res. 2000;8(5):375-85 PMID: 10997778
  10. DNA sequence evidence for the segmental allotetraploid origin of maize.
    Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6809-14 PMID: 11038553
  11. The location of 5S (ribosomal) RNA genes in Drosophila hydei.
    Chromosoma. 1975 Aug 11;51(4):347-56 PMID: 1175453
  12. Comparative genome mapping of Sorghum and maize.
    Genetics. 1992 Dec;132(4):1119-30 PMID: 1360933
  13. Molecular organization of the X chromosome in different species of the obscura group of Drosophila.
    Genetics. 1992 Mar;130(3):513-21 PMID: 1551574
  14. A Case of Rearrangement of Genes in Drosophila.
    Proc Natl Acad Sci U S A. 1921 Aug;7(8):235-7 PMID: 16576597
  15. The Relations of Inversions in the X Chromosome of Drosophila Melanogaster to Crossing over and Disjunction.
    Genetics. 1936 Sep;21(5):554-604 PMID: 17246812
  16. The Homologies of the Chromosome Elements in the Genus Drosophila.
    Genetics. 1941 Sep;26(5):517-41 PMID: 17247021
  17. The Selective Elimination of Inversion Dicentric Chromatids during Meiosis in the Eggs of Sciara Impatiens.
    Genetics. 1946 Jan;31(1):95-113 PMID: 17247187
  18. Characterization of bacteriophage P1 library containing inserts of Drosophila DNA of 75-100 kilobase pairs.
    Chromosoma. 1991 Sep;100(8):487-94 PMID: 1764967
  19. Towards a physical map of the Drosophila melanogaster genome: mapping of cosmid clones within defined genomic divisions.
    Nucleic Acids Res. 1990 Nov 11;18(21):6261-70 PMID: 2123026
  20. Bacteriophage P1 cloning system for the isolation, amplification, and recovery of DNA fragments as large as 100 kilobase pairs.
    Proc Natl Acad Sci U S A. 1990 Jan;87(1):103-7 PMID: 2404272
  21. In situ hybridization analysis of chromosomal homologies in Drosophila melanogaster and Drosophila virilis.
    Genetics. 1989 May;122(1):99-109 PMID: 2499517
  22. INVERSION LENGTH AND BREAKPOINT DISTRIBUTION IN THE DROSOPHILA BUZZATII SPECIES COMPLEX: IS INVERSION LENGTH A SELECTED TRAIT?
    Evolution. 1997 Aug;51(4):1149-1155 PMID: 28565492
  23. CHROMOSOMAL REPATTERNING AND LINKAGE GROUP CONSERVATION IN MOSQUITO KARYOTYPIC EVOLUTION.
    Evolution. 1994 Feb;48(1):146-154 PMID: 28567783
  24. Molecular evolution among some Drosophila species groups as indicated by two-dimensional electrophoresis.
    J Mol Evol. 1988;27(3):250-60 PMID: 3138427
  25. DNA sequence comparison among closely related Drosophila species in the mulleri complex.
    Genetics. 1986 Jun;113(2):287-303 PMID: 3721196
  26. Ancient linkage groups and frozen accidents.
    Nature. 1973 Aug 3;244(5414):259-62 PMID: 4200792
  27. Lengths of chromosomal segments conserved since divergence of man and mouse.
    Proc Natl Acad Sci U S A. 1984 Feb;81(3):814-8 PMID: 6583681
  28. The unusual structure of heat shock locus 2-48B in Drosophila hydei.
    Mol Gen Genet. 1984;197(3):392-8 PMID: 6597335
  29. Analysis of chromosomal homologies between two species of the subgenus Sophophora: D. miranda and D. melanogaster using cloned DNA segments.
    Chromosoma. 1982;87(1):77-88 PMID: 6819117
  30. Molecular phylogeny and divergence times of drosophilid species.
    Mol Biol Evol. 1995 May;12(3):391-404 PMID: 7739381
  31. Comparative mapping reveals extensive linkage conservation--but with gene order rearrangements--between the pig and the human genomes.
    Genomics. 1995 Feb 10;25(3):682-90 PMID: 7759103
  32. Allele-specific quantification of Drosophila engrailed and invected transcripts.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12696-700 PMID: 7809104
  33. Evolution of Hox genes.
    Annu Rev Genet. 1994;28:423-42 PMID: 7893134
  34. Mcp and Fab-7: molecular analysis of putative boundaries of cis-regulatory domains in the bithorax complex of Drosophila melanogaster.
    Nucleic Acids Res. 1994 Aug 11;22(15):3138-46 PMID: 7915032
  35. The marsupial mitochondrial genome and the evolution of placental mammals.
    Genetics. 1994 May;137(1):243-56 PMID: 8056314
  36. Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse.
    Genomics. 1993 Apr;16(1):1-19 PMID: 8486346
  37. P1 clones from Drosophila melanogaster as markers to study the chromosomal evolution of Muller's A element in two species of the obscura group of Drosophila.
    Chromosoma. 1995 Nov;104(2):129-36 PMID: 8585990
  38. Splits in fruitfly Hox gene complexes.
    Nature. 1996 Mar 14;380(6570):116 PMID: 8600383
  39. In vivo targeted mutagenesis of a regulatory element required for positioning the Hoxd-11 and Hoxd-10 expression boundaries.
    Genes Dev. 1996 Sep 15;10(18):2326-34 PMID: 8824591
  40. The stoned locus of Drosophila melanogaster produces a dicistronic transcript and encodes two distinct polypeptides.
    Genetics. 1996 Aug;143(4):1699-711 PMID: 8844157
  41. Differentiation of Muller's chromosomal elements D and E in the obscura group of Drosophila.
    Genetics. 1996 Sep;144(1):139-46 PMID: 8878680
  42. Toward a unified genetic map of higher plants, transcending the monocot-dicot divergence.
    Nat Genet. 1996 Dec;14(4):380-2 PMID: 8944014
  43. Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex.
    Genes Dev. 1996 Dec 15;10(24):3202-15 PMID: 8985188
  44. Chromosomal homology and molecular organization of Muller's elements D and E in the Drosophila repleta species group.
    Genetics. 1997 Feb;145(2):281-95 PMID: 9071584
  45. Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns.
    Genes Dev. 1997 Apr 1;11(7):900-13 PMID: 9106661
  46. The Adh-related gene of Drosophila melanogaster is expressed as a functional dicistronic messenger RNA: multigenic transcription in higher organisms.
    EMBO J. 1997 Apr 15;16(8):2023-31 PMID: 9155028
  47. Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes.
    Genetics. 1997 Jun;146(2):695-709 PMID: 9178017
  48. An episodic change of rDNA nucleotide substitution rate has occurred during the emergence of the insect order Diptera.
    Mol Biol Evol. 1997 Jun;14(6):644-53 PMID: 9190066
  49. A framework physical map of Drosophila virilis based on P1 clones: applications in genome evolution.
    Chromosoma. 1997 Jul;106(2):99-107 PMID: 9215559
  50. 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
  51. Discordant rates of chromosome evolution in the Drosophila virilis species group.
    Genetics. 1997 Sep;147(1):223-30 PMID: 9286682
  52. Synteny conservation and chromosome rearrangements during mammalian evolution.
    Genetics. 1997 Sep;147(1):289-96 PMID: 9286688
  53. On the fertility effects of pericentric inversions.
    Genetics. 1997 Oct;147(2):931-3 PMID: 9335625
  54. Comparative genomics: lessons from cats.
    Trends Genet. 1997 Oct;13(10):393-9 PMID: 9351340
  55. Construction and extensive characterization of a goat bacterial artificial chromosome library with threefold genome coverage.
    Mamm Genome. 1998 Feb;9(2):119-24 PMID: 9457672
  56. Comparative gene mapping: a fine-scale survey of chromosome rearrangements between ruminants and humans.
    Genome Res. 1998 Sep;8(9):901-15 PMID: 9750190
  57. Plant comparative genetics after 10 years.
    Science. 1998 Oct 23;282(5389):656-9 PMID: 9784118
  58. Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements.
    Genetics. 1998 Nov;150(3):1217-28 PMID: 9799273
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
DOI
10.1101/gr.162901
Email
jranz@oeb.harvard.edu
Published
2001-02-00
Pages
230-9
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC311025
Subset
IM
Databases
GENBANK
AF319441
External Links
PubMed source DOI: 10.1101/gr.162901 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