Abstract
The genes janus (Jan) A and B, and serendipity (sry) β and λ are two pairs of duplicated genes that are adjacent to each other on the third chromosome of Drosophila melanogaster. The jan A and sry β genes are expressed throughout development in both males and females. They are transcribed in opposite orientations from start sites separated by only 173 by of DNA. We report here the complete sequence of the jan A and B genes in Drosophila pseudoobscura, a species distantly related to D. melanogaster in which the overall organization of the sry β, Jan A and jan B genes is identical to that in D. melanogaster. Sequence comparison of the jan A-sry β intergenic region and 5'-transcribed domain of each gene between D. melanogaster and D. pseudoobscura reveals short stretches of conserved sequences that may correspond to cis-acting regulator elements. In order to test the possibility that some cis-acting regulatory sequences are shared by the two genes, we carried out a deletion analysis of the jan A/sry β intergenic region in D. melanogaster using transgenic lacZ fusion genes. Our results show that sry β cis-acting sequences are located in the (-117; + 137) 5′-region of the gene and that jan A cis-regulatory sequences are included in the (-56; +151) 5′-domain of this gene. Together these data indicate that in spite of the physical proximity of the jan A and sry β genes, their transcription is regulated by separate cis-acting sequences.
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Crozatier M, Kongsuwan K, Ferrer P, Merriam JR, Lengyel JA, Vincent A (1992) Single amino-acid exchanges in separate domains of the Drosophila serendipity λ zinc finger proteins cause embryonic and sex biaised lethality. Genetics 131:905–916
Dente L, Cesarini G, Cortese R (1983) pEMBL: a new family of single stranded plasmids. Nucleic Acids Res 11:1645–1655
Edgar BA, Schubiger G (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44:871–877
Ferrer P, Crozatier M, Salles C, Vincent A (1994) Interspecific comparison of Drosophila serendipity λ and β: multi-modular structure of these C2H2 zinc finger proteins. J Mol Evol 38:263–273
Fitzgerald M, Shenk T (1981) The sequence of the 5′-AAUAAA-3′ forms part of the recognition site for polyadenylation of late SV40 mRNAs. Cell 24:251–260
Garabedian MJ, Hung MC, Wensink PC (1985) Independent control elements that determine yolk protein gene expression in alternative Drosophila tissues. Proc Natl Acad Sci USA 82:1396–1400
Garabedian MJ, Shepherd BM Wensink PC (1986) A tissue-specific transcriptional enhancer from the Drosophila yolk protein 1 gene. Cell 45:859–867
Glaser RL, Lis JT (1990) Multiple, compensatory regulatory elements specify spermatocyte-specific expression of the Drosophila melanogaster hsp26 gene. Mol Cell Biol 10:131–137
Henikoff S (1987) Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods Enzymol 155:156–165
Hiromi Y, Gehring WJ (1987) Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50:963–974
Hung MC, Wensink PC (1983) Sequence and structure conservation in yolk proteins and their genes. J Mol Biol 164:481–492
Ish-Horowicz D, Howard KR, Pinchin SM, Ingham PW (1985) Molecular and genetic analysis of the hairy locus in Drosophila. Cold spring Harbor symp Quant Biol 50:135–144
Klämbt C, Jacobs JR, Goodman CS (1991) The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64:801–815
Kuhn R, Schäfer U, Schäfer M (1988) Cis-acting regions sufficient for spermatocyte-specific transcriptional and spermatid-specific translational control of the Drosophila melanogaster gene mst(3)gl-9. EMBO J 7:447–454
Kuhn R, Kuhn C, Börsch D, Glätzer KH, Schäfer U, Schäfer M (1991) A cluster of four genes selectively expressed in the male germ line of Drosophila melanogaster. Mech Dev 35:143–151
Lardelli M, Ish-Horowicz D (1993) Drosophila hairy pair-rule gene regulates embryonic patterning outside its apparent stripe domain. Development 118:255–266
Logan SK, Garabedian MJ, Wensink PC (1989) DNA regions that regulate the ovarian transcriptional specificity of Drosophila yolk protein genes. Genes Dev 3:1453–1461
Michiels F, Gasch A, Kaltschmidt B, Renkawitz-Pohl R (1989) A 14 by promoter element directs the testis specificity of the Drosophila β2 tubulin gene. EMBO J 8:1559–1565
O'Connell P, Rosbash M (1984) Sequence, structure and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res 12:5495–5513
Payre F, Yanicostas C, Vincent A (1989) serendipity delta, a Drosophila zinc finger protein present in embryonic nuclei at the onset of zygotic gene transcription. Dev Biol 136:469–480
Payre F, Noselli S, Lefrère V, Vincent A (1990) The closely related sry β and sry λ zinc finger proteins show differential embryonic expression and distinct patterns of binding sites of polytene chromosomes. Development 110:141–149
Proudfoot NJ, Brownlee GG (1976) The 3′ non-coding region sequences in eukaryotic messenger RNA. Nature 263:211–214
Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz D, Benz WK, Engels WR (1988) A stable source of P-element: transposase in Drosophila melanogaster. Genetics 118:461–470
Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218:348–353
Rushlow CA, Hogan A, Pinchin SM, Howard KR, Lardelli MT, Ish-Horowicz D (1989) The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBOJ 8:3095–3103
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Schäfer M, Börsch D, Hülster A, Schäfer U (1993) Expression of a gene duplication encoding conserved sperm tail proteins is translationally regulated in Drosophila melanogaster. Mol Cell Bio1 13:1708–1718
Schulz RA, Butler BA (1989) Overlapping genes of Drosophila melanogaster: organization of the z600-gonadal Eip28/29 gene cluster. Genes Dev 3:232–242
Schulz RA, Xie X, Miksch J (1990a) cis-acting sequences required for the germ line expression of the Drosophila gonadal gene. Dev Biol 140:455–458
Schulz RA, Miksch JL, Xie X, Cornish JA, Galewski S (1990b) Expression of the Drosophila gonadal gene: alternative promoter control germ-like expression of monocistronic and bicistronic gene transcripts. Development 108:613–622
Schweisguth F, Yanicostas C, Payre F, Lepesant JA, Vincent A (1989) Cis regulatory elements of the Drosophila blastodermspecific serendipity alpha: Ectopic activation in the embryonic PNS promoted by a deletion of an upstream element. Dev Biol 136:181–193
Segarra C, Aguadé M (1993) Nucleotide divergence of the rp 49 gene region between D. melanogaster and two species of the obscura group of Drosophila J Mol Evol 36:243–248
Shepherd BS, Garabedian MJ, Hung MC, Wensink PC (1985) Developmental control of Drosophila yolk protein 1 gene by cis-acting DNA elements. Cold Spring Harbor Symp Quant Biol 50:521–526
Vincent A, O'Connel P, Gray MR, Rosbash M (1984) Drosophila maternal and embryo mRNA transcribed from a single transcription unit use alternate combinations of exons. EMBO J 3:1003–1013
Vincent A, Colot HV, Rosbash M (1985) Sequence and structure of the serendipity locus of Drosophila melanogaster. J Mol Biol 186:149–166
Yanicostas C, Lepesant JA (1990). Transcriptional and translational cis-regulatory sequences of the spermatocyte-specific Drosophila janusB gene are located in the 3′ exonic region of the overlapping janusA gene. Mol Gen Genet 224:450–458
Yanicostas C, Vincent A, Lepesant JA (1989) Transcriptional and posttranscriptional regulation contribute to the sex-regulated expression of two sequence-related genes at the janus locus of Drosophila melanogaster. Mol Cell Biol 9:2526–2535
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Communicated by J. Campos-Ortega
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Yanicostas, C., Ferrer, P., Vincent, A. et al. Separate cis-regulatory sequences control expression of serendipity β and janus A, two immediately adjacent Drosophila genes. Molec. Gen. Genet. 246, 549–560 (1995). https://doi.org/10.1007/BF00298961
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DOI: https://doi.org/10.1007/BF00298961