How Malleable is the Eukaryotic Genome? Extreme Rate of Chromosomal Rearrangement in the GenusDrosophila
10.1101/gr.162901
Crossref journal-article
Cold Spring Harbor Laboratory
Genome Research (246)
Abstract

During the evolution of the genusDrosophila, 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 inDrosophila repleta(chromosome 2) and compared the order and distances between the markers with those on the homologous chromosomal element (3R) inDrosophila melanogaster. The two species belong to different subgenera (DrosophilaandSophophora, respectively), which diverged 40–62 million years (Myr) ago and represent, thus, the farthest lineages within theDrosophilagenus. 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 theDrosophilagenome 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 betweenD. melanogasterandD. 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 theDrosophilagenome 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 theDrosophilagenome to other insects.[The sequence data described in this paper have been submitted to the GenBank data library under accession no,AF319441.]

Bibliography

Ranz, J. M., Casals, F., & Ruiz, A. (2001). How Malleable is the Eukaryotic Genome? Extreme Rate of Chromosomal Rearrangement in the GenusDrosophila. Genome Research, 11(2), 230–239.

Authors 3
  1. José Marı́a Ranz (first)
  2. Ferran Casals (additional)
  3. Alfredo Ruiz (additional)
References 79 Referenced 134
  1. 10.1126/science.287.5461.2185
  2. 10.1007/BF00326321
  3. 10.1093/nar/25.17.3389
  4. 10.1093/genetics/143.4.1699 / Genetics / The stoned locus of Drosophila melanogaster produces a dicistronic transcript and encodes two distinct polypeptides. by Andrews (1996)
  5. 10.1007/BF02672069
  6. BDGP. 2000. The Berkeley Drosophila Genome Project database. http://www.fruitfly.org.
  7. 10.1093/oxfordjournals.jhered.a104022 / J. Hered. / Salivary chromosome maps, with a key to the banding of the chromosomes of Drosophila melanogaster. by Bridges (1935)
  8. 10.1093/emboj/16.8.2023
  9. Burnham C.R. (1980) Discussions in cytogenetics. (C.R. Burnham, MN).
  10. 10.2307/2411044
  11. 10.1126/science.285.5426.415
  12. 10.1093/genetics/31.1.95 / Genetics / The selective elimination of inversion dicentric chromatids during meiosis in the eggs of Sciara impatiens. by Carson (1946)
  13. Dear P.H. (1997) Genome mapping (Oxford University Press, New York), 1st ed.. (10.1093/oso/9780199636310.001.0001)
  14. EDGP. 2000. The European Drosophila Genome Project database. http://edgp.ebi.ac.uk.
  15. 10.1093/genetics/147.1.289 / Genetics / Synteny conservation and chromosome rearrangements during mammalian evolution. by Ehrlich (1997)
  16. 10.1093/nar/24.1.53
  17. 10.1093/oxfordjournals.molbev.a025804 / Mol. Biol. Evol. / An episodic change of rDNA nucleotide substitution rate has occurred during the emergence of the insect order Diptera. by Friedrich (1997)
  18. 10.1126/science.282.5389.656
  19. 10.1073/pnas.94.13.6809
  20. 10.1101/gad.10.18.2326
  21. 10.1073/pnas.91.26.12696
  22. 10.1023/A:1009206702214
  23. 10.1101/gad.11.7.900
  24. 10.1101/gad.10.24.3202
  25. Hartl D.L. Lozovskaya E.R. (1995) The Drosophila genome map: A practical guide . (Springer, New York).
  26. {'key': '2021111810452033000_11.2.230.26', 'first-page': '621', 'article-title': 'Maps of the salivary gland chromosomes of Drosophila melanogaster.', 'volume': '73', 'author': 'Heino', 'year': '1994', 'journal-title': 'Dros. Inform. Serv.'} / Dros. Inform. Serv. / Maps of the salivary gland chromosomes of Drosophila melanogaster. by Heino (1994)
  27. 10.1093/genetics/137.1.243 / Genetics / The marsupial mitochondrial genome and the evolution of placental mammals. by Janke (1994)
  28. 10.1016/0888-7543(95)80011-A
  29. 10.1093/nar/22.15.3138
  30. Krimbas C.B. Powell J.R. (1992) Drosophila inversion polymorphism. (CRC, Boca Raton, FL).
  31. 10.1093/genetics/150.3.1217 / Genetics / 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. by Lagercrantz (1998)
  32. Lefevre G. Jr. (1976) A photographic representation and interpretation of the polytene chromosomes of Drosophila melanogaster salivary glands. in The genetics and biology of Drosophila, ed Ashburner M. (Academic Press, London), pp 31–66.
  33. Lindsley D.L. Zimm G.G. (1992) The genome of Drosophila melanogaster. (Academic Press, San Diego).
  34. 10.1093/genetics/152.3.1183 / Genetics / Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. by Livingstone (1999)
  35. 10.1006/geno.1993.1133
  36. 10.2307/2410010
  37. Muller J.H. (1940) Bearings of the Drosophila work on systematics. in New systematic, ed Huxley J. (Clarendon Press, Oxford), pp 185–268.
  38. 10.1073/pnas.81.3.814
  39. 10.1093/genetics/147.2.931 / Genetics / On the fertility effects of pericentric inversions. by Navarro (1997)
  40. 10.1093/genetics/146.2.695 / Genetics / Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. by Navarro (1997)
  41. 10.1038/244259a0 / Nature / Ancient linkage groups and frozen accidents. by Ohno (1973)
  42. 10.1016/S0168-9525(97)01297-3
  43. 10.1126/science.286.5439.458
  44. 10.1038/ng1296-380
  45. 10.1007/BF00329934
  46. Powell J.R. (1997) Progress and prospects in evolutionary biology: The Drosophila model . (Oxford University Press, New York). (10.1093/oso/9780195076912.001.0001)
  47. 10.1093/genetics/145.2.281 / Genetics / Chromosomal homology and molecular organization of Muller's elements D and E in the Drosophila repleta species group. by Ranz (1997)
  48. 10.1007/s004120050349
  49. 10.1146/annurev.ge.28.120194.002231
  50. {'key': '2021111810452033000_11.2.230.50', 'first-page': '391', 'article-title': 'Molecular phylogeny and divergence times of Drosophilid species.', 'volume': '12', 'author': 'Russo', 'year': '1995', 'journal-title': 'Mol. Biol. Evol.'} / Mol. Biol. Evol. / Molecular phylogeny and divergence times of Drosophilid species. by Russo (1995)
  51. Sambrook J. Fritsch E.F. Maniatis T. (1989) Molecular cloning, A laboratory manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), 2nd ed..
  52. 10.1101/gr.8.9.901 / Genome Res. / Comparative gene mapping: A fine-scale survey of chromosome rearrangements between ruminants and humans. by Schibler (1998)
  53. 10.1007/s003359900701
  54. 10.1093/genetics/113.2.287 / Genetics / DNA sequence comparison among closely related Drosophila species of the mulleri complex. by Schulze (1986)
  55. 10.1093/genetics/130.3.513 / Genetics / Molecular organization of the X chromosome in different species of the obscura group of Drosophila. by Segarra (1992)
  56. {'key': '2021111810452033000_11.2.230.56', 'first-page': '129', 'article-title': "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.", 'volume': '104', 'author': 'Segarra', 'year': '1995', 'journal-title': 'Chromosoma'} / Chromosoma / 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. by Segarra (1995)
  57. 10.1093/genetics/144.1.139 / Genetics / Differentiation of Muller's chromosomal elements D and E in the obscura group of Drosophila. by Segarra (1996)
  58. 10.1093/nar/18.21.6261
  59. Smoller, D.A., Petrov, D., and Hartl, D.L. Characterization of bacteriophage P1 library containing inserts of Drosophila DNA of 75–100 kilobase pairs. Chromosoma 100: 487–494.. (10.1007/BF00352199)
  60. 10.1007/BF02100081
  61. 10.1007/BF00333510
  62. 10.1007/BF00286484 / Chromosoma / Chromosome homologies within the Drosophila obscura group probed by in situ hybridization. by Steinemann (1984)
  63. 10.1073/pnas.87.1.103
  64. 10.1002/jez.1400140104
  65. 10.1073/pnas.7.8.235
  66. 10.1093/genetics/21.5.554 / Genetics / The relations of inversions in the X chromosome of D. melanogaster to crossing over and disjunction. by Sturtevant (1936)
  67. 10.1093/genetics/26.5.517 / Genetics / The homologies of the chromosome elements in the genus Drosophila. by Sturtevant (1941)
  68. 10.1101/gr.10.5.624
  69. {'key': '2021111810452033000_11.2.230.69', 'first-page': '421', 'article-title': 'The phylogeny, ecology, and geography of Drosophila.', 'volume': '3', 'author': 'Throckmorton', 'year': '1975', 'journal-title': 'Handbook of genetics'} / Handbook of genetics / The phylogeny, ecology, and geography of Drosophila. by Throckmorton (1975)
  70. 10.1093/genetics/147.1.223 / Genetics / Discordant rates of chromosome evolution in the Drosophila virilis species group. by Vieira (1997)
  71. 10.1007/s004120050229
  72. 10.1038/380116a0
  73. Wasserman M. (1992) Cytological evolution of the Drosophila repleta species group. in Drosophila inversion polymorphism, ed Krimbas C.B. (CRC, Boca Raton, FL), pp 455–552.
  74. {'key': '2021111810452033000_11.2.230.74', 'first-page': '23', 'article-title': 'Analysis of the repleta group of Drosophila.', 'volume': '4228', 'author': 'Wharton', 'year': '1942', 'journal-title': 'University of Texas Publication.'} / University of Texas Publication. / Analysis of the repleta group of Drosophila. by Wharton (1942)
  75. White M.J.D. (1973) Animal cytology and evolution. (Cambridge University Press, London).
  76. 10.1093/genetics/122.1.99 / Genetics / In situ hybridization analysis of chromosomal homologies in Drosophila melanogaster and Drosophila virilis. by Whiting (1989)
  77. 10.1093/genetics/132.4.1119 / Genetics / Comparative genome mapping of shorgum and maize. by Whitkus (1992)
  78. 10.1007/s004380050013
  79. 10.1093/genetics/153.2.891 / Genetics / Stress sensitive B encodes an adenine nucleotide translocase in Drosophila melanogaster. by Zhang (1999)
Dates
Type When
Created 23 years, 1 month ago (July 26, 2002, 8 p.m.)
Deposited 1 year, 7 months ago (Jan. 4, 2024, 11:39 p.m.)
Indexed 3 weeks, 2 days ago (Aug. 5, 2025, 8:16 a.m.)
Issued 24 years, 6 months ago (Feb. 1, 2001)
Published 24 years, 6 months ago (Feb. 1, 2001)
Published Online 24 years, 6 months ago (Feb. 1, 2001)
Published Print 24 years, 6 months ago (Feb. 1, 2001)
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@article{Ranz_2001, title={How Malleable is the Eukaryotic Genome? Extreme Rate of Chromosomal Rearrangement in the GenusDrosophila}, volume={11}, ISSN={1549-5469}, url={http://dx.doi.org/10.1101/gr.162901}, DOI={10.1101/gr.162901}, number={2}, journal={Genome Research}, publisher={Cold Spring Harbor Laboratory}, author={Ranz, José Marı́a and Casals, Ferran and Ruiz, Alfredo}, year={2001}, month=feb, pages={230–239} }