Comparative genome sequencing of Drosophila pseudoobscura: Chromosomal, gene, and cis-element evolution (original) (raw)

  1. Stephen Richards1,15,
  2. Yue Liu1,2,3,
  3. Brian R. Bettencourt4,
  4. Pavel Hradecky4,
  5. Stan Letovsky4,
  6. Rasmus Nielsen5,
  7. Kevin Thornton5,
  8. Melissa J. Hubisz5,
  9. Rui Chen1,
  10. Richard P. Meisel6,
  11. Olivier Couronne8,12,
  12. Sujun Hua9,
  13. Mark A. Smith4,
  14. Peili Zhang4,
  15. Jing Liu1,
  16. Harmen J. Bussemaker10,
  17. Marinus F. van Batenburg10,13,
  18. Sally L. Howells1,
  19. Steven E. Scherer1,
  20. Erica Sodergren1,
  21. Beverly B. Matthews4,
  22. Madeline A. Crosby4,
  23. Andrew J. Schroeder4,
  24. Daniel Ortiz-Barrientos11,
  25. Catharine M. Rives1,
  26. Michael L. Metzker1,
  27. Donna M. Muzny1,
  28. Graham Scott1,
  29. David Steffen1,
  30. David A. Wheeler1,
  31. Kim C. Worley1,
  32. Paul Havlak1,
  33. K. James Durbin1,
  34. Amy Egan1,
  35. Rachel Gill1,
  36. Jennifer Hume1,
  37. Margaret B. Morgan1,
  38. George Miner1,
  39. Cerissa Hamilton1,
  40. Yanmei Huang4,
  41. Lenée Waldron1,
  42. Daniel Verduzco1,
  43. Kerstin P. Clerc-Blankenburg1,
  44. Inna Dubchak8,
  45. Mohamed A.F. Noor11,
  46. Wyatt Anderson14,
  47. Kevin P. White9,
  48. Andrew G. Clark5,
  49. Stephen W. Schaeffer7,
  50. William Gelbart4,
  51. George M. Weinstock1, and
  52. Richard A. Gibbs1
  53. 1 Human Genome Sequencing Center and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston Texas 77030, USA
  54. 2 Program in Structural and Computational Biology and Molecular Biophysics, Baylor College of Medicine, Houston Texas 77030, USA
  55. 3 W.M. Keck Center for Computational Biology, Baylor College of Medicine, Houston Texas 77030, USA
  56. 4 FlyBase–Harvard, Department of Molecular and Cellular Biology, Harvard University, Biological Laboratories, Cambridge, Massachusetts 021383, USA
  57. 5 Department of Biological Statistics and Computational Biology, and Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853, USA
  58. 6 Intercollege Graduate Degree Program in Genetics, The Pennsylvania State University, University Park, Pennsylvania 16802, USA
  59. 7 Department of Biology and Institute of Molecular Evolutionary Genetics, The Pennsylvania State University, University Park, Pennsylvania 16802, USA
  60. 8 Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA
  61. 9 Department of Genetics, Yale University School of Medicine, New Haven, Connecticut 06520, USA
  62. 10 Department of Biological Sciences and Center for Computational Biology and Bioinformatics, Columbia University, New York, New York 10027, USA
  63. 11 Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803, USA
  64. 12 U.S. Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA
  65. 13 Swammerdam Institute for Life Sciences, University of Amsterdam, The Netherlands
  66. 14 Department of Genetics, University of Georgia, Athens, Georgia 30602, USA

Abstract

We have sequenced the genome of a second Drosophila species, Drosophila pseudoobscura, and compared this to the genome sequence of Drosophila melanogaster, a primary model organism. Throughout evolution the vast majority of Drosophila genes have remained on the same chromosome arm, but within each arm gene order has been extensively reshuffled, leading to a minimum of 921 syntenic blocks shared between the species. A repetitive sequence is found in the D. pseudoobscura genome at many junctions between adjacent syntenic blocks. Analysis of this novel repetitive element family suggests that recombination between offset elements may have given rise to many paracentric inversions, thereby contributing to the shuffling of gene order in the D. pseudoobscura lineage. Based on sequence similarity and synteny, 10,516 putative orthologs have been identified as a core gene set conserved over 25–55 million years (Myr) since the pseudoobscura/melanogaster divergence. Genes expressed in the testes had higher amino acid sequence divergence than the genome-wide average, consistent with the rapid evolution of sex-specific proteins. _Cis_-regulatory sequences are more conserved than random and nearby sequences between the species—but the difference is slight, suggesting that the evolution of _cis_-regulatory elements is flexible. Overall, a pattern of repeat-mediated chromosomal rearrangement, and high coadaptation of both male genes and _cis_-regulatory sequences emerges as important themes of genome divergence between these species of Drosophila.

Footnotes