Abstract
A clone isolated from a Drosophila auraria heat-shock cDNA library presents two long, antiparallel, coupled (LAC) open reading frames (ORFs). One strand ORF is 1,929 nucleotides long and exhibits great identity (87.5% at the nucleotide level and 94% at the amino acid level) with the hsp70 gene copies of D. melanogaster, while the second strand ORF, in antiparallel in-frame register arrangement, is 1,839 nucleotides long and exhibits 32% identity with a putative, recently identified, NAD+-dependent glutamate dehydrogenase (NAD+-GDH). The overlap of the two ORFs is 1,824 nucleotides long. Computational analysis shows that this LAC ORF arrangement is conserved in other hsp70 loci in a wide range of organisms, raising questions about possible evolutionary benefits of such a peculiar genomic organization.
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References
Adelman JP, Bond CT, Douglass J, Herbert E (1987) Two mammalian genes transcribed from opposite strands of the same DNA locus. Science 235:1514–1517
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Aviv H, Leder P (1972) Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci USA 69:1408–1412
Bairoch A (1992) PROSITE: a dictionary of sites and patterns in proteins. Nucleic Acids Res 20:2013–2018
Bairoch A, Boeckmann B (1992) The SWISS-PROT protein sequence data bank. Nucleic Acids Res 20:2019–2022
Benachenhou-Lahfa N, Forterre P, Labedan B (1993) Evolution of glutamate dehydrogenase genes: evidence for two paralogous protein families and unusual branching patterns of the archaebacteria in the universal tree of life. J Mol Evol 36:335–346
Boles E, Zimmermann FK (1994) Open reading frames in the antisense strands of genes coding for glycolytic enzymes in Saccharomyces cerevisiae. Mol Gen Genet 243:363–368
Boorstein RW, Ziegelhoffer T, Craig EA (1994) Molecular evolution of the HSP70 multigene family. J Mol Evol 38:1–17
Bork P, Ouzounis C, Sander C, Scharf M, Schneider R, Sonnhammer E (1992) Comprehensive sequence analysis of the 182 predicted open reading frames of yeast chromosome III. Protein Sci 1:1677–1690
Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium cyanate-phenol-chlorophorm extraction. Anal Biochem 162:156–159
Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995
Clark MW, Keng T, Storms RK, Zhong W, Fortin N, Zeng B, Delaney S, Ouellette FBF, Barton AB, Kaback DB, Bussey H (1994) Sequencing of chromosome I of Saccharomyces cerevisiae: analysis of the 42 Kbp SP07-CENI-CDC15 region. Unpublished
Feinberg AP, Fogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13
Felsenstein J (1988) PHYLIP: phylogeny inference package. Cladistics 5:355–356
Flaherty KM, De Luca-Flaherty CR, McKay DB (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346:623–628
Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R (1981) Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res 9:r43-r74
Henikoff S, Keene MA, Fechtel K, Fristrom JW (1986) Gene within a gene: nested Drosophila genes encode unrelated proteins on opposite DNA strands. Cell 44:33–42
Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci 8:189–191
Kastritsis CD, Scouras ZG, Ashburner M (1986) Duplications in the polytene chromosomes of Drosophila auraria. Chromosoma 93: 381–385
LeJohn HB, Cameron LE, Yang B, Rennie SL (1994) Molecular characterization of an NAD-specific glutamate dehydrogenase gene inducible by L-glutamine: antisense gene pair arrangement with L-glutamine-inducible heat shock 70-like protein gene. J Biol Chem 269:4523–4531
Lemeunier F, David JR, Tsacas L, Ashburner M (1986) The melanogaster species group. In: Ashburner M, Carson HL, Thompson J (eds) The genetics and biology of Drosophila. Academic Press, London. vol 3, pp 147–256
Lindquist S, Craig EA (1988) The heat shock proteins. Annu Rev Genet 22:631–677
Merino E, Balbas P, Puente JL, Bolivar F (1994) Antisense overlapping open reading frames in genes from bacteria to humans. Nucleic Acid Res 22:1903–1908
Papadopoulou D, Louis C (1990) The gene coding for glutamate dehydrogenase in Drosophila melanogaster. Biochem Genet 28:337–346
Parsell DA, Lindquist S (1993) The function of heat shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496
Perkins LA, Doctor JS, Zhang K, Stinson L, Perrimon N, Craig EA (1990) Molecular and developmental characterization of the heat shock cognate 4 gene of Drosophila melanogaster. Mol Cell Biol 10:3232–3238
Pissios P, Scouras ZG (1993) Mitochondrial DNA evolution in the montium species subgroup of Drosophila. Mol Biol Evol 10:37–5382
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Schedl P, Artavanis-Tsakonas S, Steward R, Gehring WJ, Mirault M-E, Goldschmidt-Clermont M, Moran L, Tissieres A (1978) Two hybrid plasmids with Drosophila melanogaster DNA sequences complementary to mRNA coding for the major heat shock protein. Cell 14:921–929
Scouras ZG, Kastritsis CD (1984) Balbiani rings and puffs of the polytene chromosomes of Drosophila auraria. Chromosoma 89:96–106
Scouras ZG, Karamanlidou GA, Kastritsis CD (1986) The influence of heat shock on the puffing pattern of Drosophila auraria polytene chromosomes. Genetica 69:13–218
Scouras ZG, Milioni D, Yiangou M, Duchene M, Domdey H (1994) The β-tubulin genes of Drosophila auraria are arranged in a cluster. Curr Genet 25:84–87
Spencer CA, Gietz RD, Hodgetts RB (1986) Overlapping transcription units in the dopa decarboxylase region of Drosophila. Nature 322: 279–281
Thompson-Jäger S, Domdey H (1990) The intron of the yeast actin gene contains the promoter for the antisense RNA. Curr Genet 17:269–273
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Correspondence to: Z.G. Scouras
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Konstantopoulou, I., Ouzounis, C.A., Drosopoulou, E. et al. A Drosophila hsp70 gene contains long, antiparallel, coupled open reading frames (LAC ORFs) conserved in homologous loci. J Mol Evol 41, 414–420 (1995). https://doi.org/10.1007/BF00160312
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DOI: https://doi.org/10.1007/BF00160312