Summary
The Cs gene lies between the functionally and evolutionarily related dopa decarboxylase (Ddc) and l(2) amd loci of Drosophila. The Cs and Ddc genes overlap at their 3′ ends, implying that the transcription termination signals of these genes are polar, since each gene's primary transcript contains the complement of the other gene's transcription termination signals. The mature transcripts of the Cs and Ddc genes are complementary for a short distance and the primary transcripts may be complementary over thousands of base pairs. Despite intensive mutagenesis in this region, no mutations affecting the Cs transcript have been recovered although over 90 alleles of the two flanking genes (Ddc and l(2) amd) have been identified. Unlike the flanking Ddc and l(2) amd genes, the structure of the Cs gene and the temporal and tissue specificity of Cs expression are inconsistent with any structural or functional relatedness to the Ddc gene family. The internal structure of the Cs transcript is unlike that of most protein coding genes; it contains several open reading frames which are not situated favorably for efficient translation of the Cs message. This unusual internal structure may be the basis of the observed mutational silence of the Cs locus.
Similar content being viewed by others
References
Beall CJ, Hirsh J (1986) Drosophila melangaster Ddc gene trascripts are not expressed at high levels during early embryogenesis. Dev Biol 114:258–259
Birnstiel ML, Busslinger M, Strub K (1985) Transcription termination and 3′ processing: the end is in site. Cell 41:349–359
Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383
Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
Eveleth DD, Marsh JL (1986a) Sequence and expression of the Cc gene, a member of the dopa decarboxylase gene cluster of Drosophila: possible translational regulation. Nucleic Acids Res 14:6169–6183
Eveleth DD, Marsh JL (1986b) Evidence for evolutionary duplication of genes in the dopa decarboxylase region of Drosophila. Genetics 114:469–483
Eveleth DD, Gietz RD, Spencer CA, Nargang F, Hodgetts RB, Marsh JL (1986) Sequence and structure of the dopa decarboxylase gene of Drosophila: evidence for novel RNA splicing variants. EMBO J
Falk-Pederson E, Logan J, Shenk T, Darnell JE Jr (1985) Transcription termination within the E1A gene of Adenovirus induced by insertion of the mouse β-globin terminator element. Cell 40:897–905
Garbe JC, Pardue ML (1986) Heat shock locus 93D of Drosophila melanogaster: A spliced RNA most strongly conserved in the intron sequence. Proc Natl Acad Sci USA 83:1812–1816
Gilbert D, Hirsh J, Wright TRF (1984) Molecular mapping of a gene cluster flanking the Drosophila dopa decarboxylase gene. Genetics 106:679–694
Gribskov M, Devereux J, Burgess RR (1984) The codon usage plot: graphic analysis of protein coding sequences and prediction of gene expression. Nucleic Acids Res 12:539–549
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
Hirsh J, Davidson N (1981) Isolation and characterization of the dopa decarboxylase gene of Drosophila melanogaster. Mol Cell Biol 1:475–485
Kozak M (1981) Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucleic Acids Res 9:5233–5247
Maniatis T, Hardison RC, Lacy E, Lauer J, O'Connell D, Quon D, Sim GK, Efstratiadis A (1978) Isolation of structural genes from libraries of eukaryotic DNA. Cell 15:687–701
Marsh JL, Wright TRF (1986) Evidence for regulatory variants of the dopa decarboxylase and alpha methyl dopa hypersensitive loci in Drosophila. Genetics 112:249–265
Marsh JL, Gibbs PDL, Timmons P (1985) Developmental control of transduced dopa decarboxylase genes in Drosophila melanogaster. Mol Gen Genet 198:393–403
Marsh JL, Erfle MP, Leeds CA (1986) Developmental expression and nucleotide sequence of the alpha methyl dopa hypersensitive gene of Drosophila. Genetics
Maruyama T, Gobujori T, Aota S, Ikemura T (1986) Codon usage tabulated from the GenBank genetic sequence data. Nucleic Acids Res 14:151–197
McLaughlan J, Gaffney D, Whitton JL, Clements JB (1985) The consensus sequence YGTGTTYYY located downstream from the AATAAA signal is required for efficient formation of mRNA 3′ termini. Nucleic Acids Res 13:1347–1360
Messing J (1983) New M13 vectors for cloning. Methods 101:20–78
Pentz ES, Wright TRF (1986) A diphenol oxidase gene is part of a cluster of genes involved in catecholamine metabolism and sclerotization in Drosophila II: Molecular localization of the Dox-A2 coding region. Genetics 112:843–859
Sanger F, Nicklen S, Coulsen AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Schwindinger WF, Warner JR (1984) DNA sequence analysis on the IBM PC. Nucleic Acids Res 12:601–604
Sharp PM, Rogers MS, McConnell DJ (1985) Selection pressures on codon usage in the complete genome of bacteriophage T7. J Mol Evol 21:150–160
Sharp PM, Tuohy TMF, Mosurski KR (1986) Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res 14:5125–5143
Spencer CA, Gietz RD, Hodgetts RB (1986a) Analysis of the transcription unit adjacent to the 3′ end of the dopa decarboxylase gene in Drosophila melanogaster. Dev Biol 114:260–264
Spencer CA, Gietz RD, Hodgetts RB (1986b) Overlapping transcription units in the dopa decarboxylase region of Drosophila. Nature 322:279–281
Williams T, Fried M (1986) A mouse locus at which transcription from both DNA strands produces mRNAs complementary at their 3′ ends. Nature 322:275–279
Wright TRF, Beermann W, Marsh JL, Bishop CB, Steward R, Black BC, Tomsett AD, Wright EY (1981) Chromosoma 83:45–58
Wright TRF, Black B, Bishop CP, Marsh JL, Pentz ES, Steward R, Wright EY (1982) The genetics of dopa decarboxylase in Drosophila melanogaster IV. Ddc and l(2) amd alleles: isolation, characterization and intragenic complementation. Mol Gen Genet 188:18–26
Author information
Authors and Affiliations
Additional information
Communicated by R.B. Goldberg
Rights and permissions
About this article
Cite this article
Eveleth, D.D., Marsh, J.L. Overlapping transcription units in Drosophila: Sequence and structure of the Cs gene. Molec Gen Genet 209, 290–298 (1987). https://doi.org/10.1007/BF00329656
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00329656