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Molecular organization of the Drosophila melanogaster Adh chromosomal region in D. replete and D. buzzatii, two distantly related species of the Drosophila subgenus

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Abstract

The molecular organization of a 1.944-Mb chromosomal region of Drosophila melanogaster around the Adh locus has been analyzed in two repleta group species: D. repleta and D. buzzatii. The extensive genetic and molecular information about this region in D. melanogaster makes it a prime choice for comparative studies of genomic organization among distantly related species. A set of 26 P1 phages from D. melanogaster were successfully hybridized using fluorescence in-situ hybridization (FISH) to the salivary gland chromosomes of both repleta group species. The results show that the Adh region is distributed in D. repleta and D. buzzatii over six distant sites of chromosome 3, homologous to chromosomal arm 2L of D. melanogaster (Muller's element B). This observation implies a density of 2.57 fixed breakpoints per Mb in the Adh region and suggests a considerable reorganization of this chromosomal element via the fixation of paracentric inversions. Nevertheless, breakpoint density in the Adh region is three times lower than that estimated for D. repleta chromosome 2, homologous to D. melanogaster 3R (Muller's element E). Differences in the rate of evolution among chromosomal elements are seemingly persistent in the Drosophila genus over long phylogenetic distances.

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References

  • Adams MD, Celniker SE, Holt RA et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185–2195.

    Article  PubMed  Google Scholar 

  • Albalat R, González-Duarte R (1993) Adh and Adh-dup sequences of Drosophila lebanonensis and D. immigrans: interspecies comparisons. Gene 126: 171–178.

    Article  PubMed  CAS  Google Scholar 

  • Amador A, Juan E (1999) Non fixed duplication containing the Adh gene and a truncated form of the Adhr gene in the Drosophila funebris species group: different modes of evolution of Adh relative to Adhr in Drosophila. Mol Biol Evol 16: 1439–1456.

    PubMed  CAS  Google Scholar 

  • Ashburner M, Misra S, Roote J et al. (1999) An exploration of the sequence of a 2.9–Mb region of the genome of Drosophila melanogaster. The Adh region. Genetics 153: 179–219.

    PubMed  CAS  Google Scholar 

  • BDGP (1999) Berkeley Drosophila Genome Project. Available at hhttp://www.fruitfly.orgi.

  • Begun DJ (1997) Origin and evolution of a new gene descendent from alcohol dehydrogenase in Drosophila. Genetics 145: 375–382.

    PubMed  CAS  Google Scholar 

  • Betrán E, Santos M, Ruiz A (1998) Antagonistic pleiotropic effect of second-chromosome inversions on body size and early life-history traits in Drosophila buzzatii. Evolution 52: 144–154.

    Article  Google Scholar 

  • Beverly SM, Wilson AC (1984) Molecular evolution in Drosophila and higher Dipterans. II. A time scale for fly evolution. J Mol Evol 21: 1–13.

    Article  Google Scholar 

  • Brogna S, Ashburner M (1997) The Adh-related gene of Drosophila melanogaster is expressed as a functional dicistronic messenger RNA: Multigenic transcription in higher organisms. EMBO J 16: 2023–2031.

    Article  PubMed  CAS  Google Scholar 

  • Cáceres M, Ranz JM, Barbadilla A, Long M, Ruiz A (1999) Generation of a widespread Drosophila inversion by a transposable element. Science 285: 415–418.

    Article  PubMed  Google Scholar 

  • Cirera S, Martín-Campos JM, Segarra C, Aguadé M (1995) Molecular characterization of the breakpoints of an inversion fixed between Drosophila melanogaster and Drosophila subobscura. Genetics 139: 321–326.

    PubMed  CAS  Google Scholar 

  • Grell EH, Jacobson KB, Murphy JB (1968) Alterations of gen-etic material for analysis of alcohol dehydrogenase isozymes of Drosophila melanogaster. Ann NY Acad Sci 151: 441–455.

    PubMed  CAS  Google Scholar 

  • Hartl DL, Lozovskaya ER (1994) Genome evolution: between the nucleosome and the chromosome. In: Schierwater B, Streit B, Wagner GP, de Salle R, ed. Molecular Ecology and Evolution: Approaches and Applications. Basel: Birkäser, pp 579–592.

    Google Scholar 

  • Hooper JE, Perez-Alonso M, Bermingham JR et al. (1992) Comparative studies of Drosophila Antennapedia genes. Genetics 132: 453–469.

    PubMed  CAS  Google Scholar 

  • Jeffs PS, Holmes EC, Ashburner M (1994) The molecular evol-ution of the alcohol dehydrogenase and alcohol dehydrogenase-related genes in the Drosophila melanogaster species subgroup. Mol Biol Evol 11: 287–304.

    PubMed  CAS  Google Scholar 

  • Juan E, Papaceit M, Quintana A (1994) Nucleotide sequence of the genomic region encompassing Adh and Adh-dup genes of D. lebanonensis (Scaptodrosophila): gene expression and evolutionary relationships. J Mol Evol 38: 455–467.

    Article  PubMed  CAS  Google Scholar 

  • Kress H (1993) The salivary gland chromosomes of Drosophila virilis: a cytological map, pattern of transcription and aspects of chromosome evolution. Chromosoma 102: 734–742.

    Article  PubMed  CAS  Google Scholar 

  • Labrador M, Naveira H, Fontdevila A (1990) Genetic mapping of the Adh locus in the repleta group of Drosophila by in situ hybridization. J Hered 81(1): 83–86.

    PubMed  CAS  Google Scholar 

  • Lefevre G Jr (1976) A photographic representation and interpretation of the polytene chromosomes of D. melanogaster salivary glands. In: Ashburner M, Novitski E, eds. The Genetics and Biology of Drosophila, vol. 1a. London: Academic Press, pp 31–66.

    Google Scholar 

  • Lemeunier F, Aulard S (1992) Inversion polymorphism in Drosophila melanogaster. In: Krimbas CB, Powell JR, eds. Drosophila Inversion Polymorphism. Boca Raton, Florida: CRC Press, pp 339–405.

    Google Scholar 

  • Loukas M, Kafatos FC (1986) The actin loci in the genus Drosophila: establishment of chromosomal homologies among distantly related species by in situ hybridization. Chromosoma 94: 297–308.

    Article  CAS  Google Scholar 

  • Maier D, Marte BM, Schafer W, Yu Y, Preiss A (1993) Drosophila evolution challenges postulated redundancy in the E(spl) gene complex. Proc Natl Acad Sci USA 90: 5464–5468.

    Article  PubMed  CAS  Google Scholar 

  • Marfany G, González-Duarte R (1991) The Adh genomic region of Drosophila ambigua: evolutionary trends in different species. J Mol Evol 32: 454–462.

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Cruzado JC, Swimmer MG, Fenerjian MG, Kafatos FC (1988) Evolution of the autosomal chorion locus in Drosophila. I. General organization of the locus and sequence comparisons of genes s15 and s19 in evolutionary distant species. Genetics 119: 663–677.

    PubMed  CAS  Google Scholar 

  • Menotti-Raymond M, Starmer WT, Sullivan DT (1991) Characterization of the structure and evolution of the Adh region of Drosophila hydei. Genetics 127: 355–366.

    PubMed  CAS  Google Scholar 

  • Montgomery E, Charlesworth B, Langley CH (1987) A test for role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res 49: 31–41.

    Article  PubMed  CAS  Google Scholar 

  • Muller JH (1940) Bearings of the Drosophila work on systematics. In: Huxley J, ed. New Systematics. Oxford: Clarendon Press, pp 185–268.

    Google Scholar 

  • Nadeau JH, Taylor BA (1984) Lengths of chromosomal segments conserved since divergence of man and mouse. Proc Natl Acad Sci USA 81: 814–818.

    Article  PubMed  CAS  Google Scholar 

  • Nurminsky DI, Moriyama EN, Lozovskaya ER, Hartl DL (1996) Molecular phylogeny and genome evolution in the Drosophila virilis species group: duplication of the alcohol dehydrogenase gene. Mol Biol Evol 13: 132–149.

    PubMed  CAS  Google Scholar 

  • Randazzo FM, Seeger MA, Huss CA, Sweeney MA, Cecil JK (1993) Structural changes in the Antennapedia complex of Drosophila pseudoobscura. Genetics 133: 319–330.

    Google Scholar 

  • Ranz JM, Segarra C, Ruiz A (1997) chromosomal homology and molecular organization of Muller's element D and E in the Drosophila repleta species group. Genetics 145: 281–295.

    PubMed  CAS  Google Scholar 

  • Ranz JM, Cáceres M, Ruiz A (1999) Comparative mapping of cosmids and gene clones from a 1.6 Mb chromosomal region of D. melanogaster in three species of the distantly related subgenus Drosophila. Chromosoma 108: 32–43.

    Article  PubMed  CAS  Google Scholar 

  • Ruiz A, Wasserman M (1993) Evolutionary cytoGenetics of the Drosophila buzzatii species complex. Heredity 70: 582–596.

    PubMed  Google Scholar 

  • Ruiz A, Ranz JM, Cáceres M, Segarra C, Navarro A, Barbadilla A (1997) chromosomal evolution and comparative gene mapping in the Drosophila repleta species group. Brazilian J Genet 20: 553–565.

    CAS  Google Scholar 

  • Russo CAM, Takezaki N, Nei M (1995) Molecular phylogeny and divergence times of Drosophilid species. Mol Biol Evol 12: 391–404.

    PubMed  CAS  Google Scholar 

  • Schafer DJ (1992) Developmental and molecular studies of Adh in Drosophila buzzatii. Master Thesis, University of New England Armidale, NSW, Australia.

    Google Scholar 

  • Schafer DJ, Fredline DK, Knibb WR, Green MM, Barker JSF (1993) Genetics and linkage mapping of Drosophila buzzatii. J Hered 84: 188–194.

    PubMed  CAS  Google Scholar 

  • Schneuwly S, Kuroiwa A, Gehring WJ (1987) Molecular analy-sis of the dominant homeotic Antennapedia phenotype. EMBO J 6: 201–206.

    PubMed  CAS  Google Scholar 

  • Segarra C, Aguadé M (1992) Molecular organization of the X chromosome in different species of the obscura group of Drosophila. Genetics 130: 513–521.

    PubMed  CAS  Google Scholar 

  • Segarra C, Lozovskaya ER, Ribó G, Aguadé M, Hartl DL (1995) 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 104: 129–136.

    PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf, FJ (1995) Biometry. New York: Freeman.

    Google Scholar 

  • Stathakis DS, Pentz ES, Freeman ME (1995) The genetic and molecular organization of the dopa decarboxilase gene cluster of Drosophila melanogaster. Genetics 141: 629–655.

    PubMed  CAS  Google Scholar 

  • Steineman UM (1982) Analysis of chromosomal homologies between two species of the subgenus Sophophora: D. miranda and D. melanogaster using cloned DNA segments. Chromosoma 87: 77–88.

    Article  Google Scholar 

  • Steineman UM, Pinkser W, Sperlich D (1984) Chromosome homologies within the Drosophila obscura group probed by in situ hybridization. Chromosoma 91: 46–53.

    Article  Google Scholar 

  • Sturtevant AH, Novitski E (1941) The homologies of the chromosome elements in the genus Drosophila. Genetics 26: 517–541.

    CAS  PubMed  Google Scholar 

  • Sullivan DT, Atkinson PW, Starmer WT (1990) Molecular evolution of the alcohol dehydrogenase genes in the genus Drosophila. Evolut Biol 24: 107–147.

    CAS  Google Scholar 

  • Sullivan DT, Starmer WT, Curtiss SW, Menotti-Raymond M, Yum J (1994) Unusual molecular evolution of an Adh pseudogen in Drosophila. Mol Biol Evol 11: 443–458.

    PubMed  CAS  Google Scholar 

  • Throckmorton LH (1982) The virilis species group. In: Ashburner M, Carson HL, Thompson JN eds. The Genetics and Biology of Drosophila, vol. 3b. New York: Academic Press, pp 227–296.

    Google Scholar 

  • Vieira J, Vieira CP, Hartl DL, Lozovskaya ER (1997) A frame-work physical map of D. virilis based on P1 clones: applications in genome evolution. Chromosoma 106: 99–107.

    Article  PubMed  CAS  Google Scholar 

  • Von Allmen G, Hogga I, Spierer A et al. (1996) Splits in fruitfly Hox gene complexes. Nature 380: 116.

    Article  PubMed  CAS  Google Scholar 

  • Wasserman M (1992) Cytological evolution of the Drosophila repleta species group. In: Krimbas CB, Powell JR, eds. Drosophila Inversion Polymorphism. Boca Raton, Florida: CRC Press, pp 455–552.

    Google Scholar 

  • Wharton LT (1942) Analysis of the repleta group of Drosophila. Univ Texas Publ 4228: 23–52.

    Google Scholar 

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Authors and Affiliations

  1. Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK

    Josefa González, Esther Betrán & Michael Ashburner

  2. Department de Genètica i de Microbiologia, Facultat de Ciències, Edifici C, Universitat Autònoma de Barcelona, 08193 Bellaterra, (Barcelona), Spain.

    Alfredo Ruiz

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  1. Josefa González
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  2. Esther Betrán
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  3. Michael Ashburner
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  4. Alfredo Ruiz
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González, J., Betrán, E., Ashburner, M. et al. Molecular organization of the Drosophila melanogaster Adh chromosomal region in D. replete and D. buzzatii, two distantly related species of the Drosophila subgenus. Chromosome Res 8, 375–385 (2000). https://doi.org/10.1023/A:1009206702214

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