Abstract
During early embryogenesis of Drosophila the spatial and temporal expression patterns of the region-specific homeotic gene spalt (sal) and the neighbouring gene spalt adjacent (sala) extensively overlap. We show that the initial expression patterns of the two genes in the blastoderm also have identical genetic controls. However, while sal encodes a transcription factor, sala encodes a precursor protein from which a functional signal peptide is cleaved off to generate the secreted sala protein. Ectopic expression or absence of sala protein does not affect embryonic development, adult viability or fertility. In addition to sal and sala, we identified a third gene nearby, termed spalt related (salr), which shares coding sequence similarity and a late embryonic expression pattern with sal, but lacks the early expression domains that are shared by sal and sala. These results suggest that the three genes and their present cis-regulatory regions arose through a chromosomal rearrangement involving local duplication and transposition events in the 32F/33A region on the left arm of the second chromosome.
Similar content being viewed by others
References
Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101:1–22
Berleth T, Burri M, Thoma G, Bopp D, Richstein S, Frigerio G, Noll M, Nüsslein-Volhard C (1988) The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J 7:1749–1756
Blumberg B, MacKrell AJ, Fessler JH (1988) Drosophila basement membrane procollagen al(IV). J Biol Chem 263:18328–18337
Brönner G, Jäckle H (1991) Control and function of terminal gap gene activity in the posterior pole region of the Drosophila embryo. Mech Dev 35:205–211
Bunch TA, Grinblat Y, Goldstein LSB (1988) Characterisation and use of the Drosophila methallothionin promoter in cultured Drosophila melanogaster cells. Nucleic Acids Res 16:1043–1061
Cadigan KM, Grossniklaus U, Gehring WJ (1994) Functional redundancy: The respective roles of the two sloppy paired genes in Drosophila segmentation. Proc Natl Acad Sci USA 91:6324–6328
Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin
Coleman KG, Poole SJ, Weir MP, Soeller WC, Kornberg T (1987) The invected gene of Drosophila: sequence analysis and expression studies reveal a close kinship to the engrailed gene. Genes Dev 1:19–28
Driever W, Nüsslein-Volhard C (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54:83–93
Fortini ME, Simon MA, Rubin GM (1992) Signalling by the sevenless protein tyrosine kinase is mimicked by Rasl. activation. Nature 355:559–561
Frei E, Schuh R, Baumgartner S, Burri M, Noll M, Jürgens G, Seifert E, Nauber U, Jäckle H (1988) Molecular characterization of spalt, a homeotic gene required for head and tail development in the Drosophila embryo. EMBO J 7:197–204
Gaul U, Jäckle H (1987) Pole region-dependent repression of the Drosophila gap gene Krüppel by maternal gene products. Cell 51:549–555
Gaul U, Mardon G, Rubin GM (1992) A putative Ras GTPase activating protein acts as a negative regulator of signaling by the Sevenless receptor tyrosine kinase. Cell 68:1007–1019
Gonzáles-Gaitán M, Rothe M, Wimmer EA, Taubert H, Jäckle H (1994) Redundant functions of the gene knirps and knirps-related for the establishment of anterior Drosophila head structures. Proc Natl Acad Sci USA 91:8567–8571
Grossniklaus U, Kurth-Pearson R, Gehring WJ (1992) The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev 6:1030–1051
Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683–4690
Hoch M, Gerwin N, Taubert H, Jäckle H (1992) Competition for overlapping sites in the regulatory region of the Drosophila gene Krüppel. Science 256:94–97
Ingham PW (1988) The molecular genetic of embryonic pattern formation in Drosophila. Nature 335:25–34
Jäckle H, Sauer F (1993) Transcriptional cascades in Drosophila. Curr Opin Cell Biol 5:505–512
Jackson RC, Blobel G (1977) Post-translational cleavage of presecretory proteins with an extract of rough microsomes from dog pancreas containing signal peptide activity. Proc Natl Acad Sci USA 74:5598–5602
Jürgens G (1988) Head and tail development of the Drosophila embryos involves spalt a novel homeotic gene. EMBO J 7:189–196
Klingler M, Erdéli M, Szabad J, Nüsslein-Volhard C (1988) Function of torso in determining the terminal anlagen of the Drosophila embryo. Nature 335:275–277
Krumlauf R (1994) Hox genes in vertebrate development. Cell 78:191–201
Kühnlein RP, Frommer G, Friedrich M, Gonzalez-Gaitan M, Weber A, Wagner-Bernholz JF, Gehring WJ, Jäckle H, Schuh R (1994) spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J 13:168–179
Lehmann R, Nüsslein-Volhard C (1991) The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development 112:679–691
Li X, Noll M (1994a) Compatibility between enhancers and promoters determines the transcriptional specificity of gooseberry and gooseberry neuro in the Drosophila embryo. EMBO J 13:400–406
Li X, Noll M (1994b) Evolution of distinct developmental functions of three Drosophila gene by acquisition of different cisregulatory regions. Nature 367:83–87
Manoukian AS, Krause HM (1992) Concentration-dependent activities of the even-skipped protein in Drosophila embryos. Genes Dev 6:1740–1751
Nüsslein-Volhard C, Wieschaus E, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster I: Zygotic loci on the second chromosome. Rouxs Arch Dev Biol 193:267–282
Pankratz MJ, Jäckle H (1990) Making stripes in the Drosophila embryo. Trends Genet 6:287–292
Perkins LA, Larsen I, Perrimon N (1992) corkscrew encodes a putative protein tyrosine phosphatase that functions to transduce the terminal signal from the receptor tyrosine kinase torso. Cell 70:225–236
Reuter D (1990) PhD Thesis, University of Tübingen, Tübingen, Germany
Roth S, Stein D, Nüsslein-Volhard C (1989) A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell 59:1189–1202
Rothe M, Nauber U, Jäckle H (1989) Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J 8:3087–3094
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
Sanger F, Nicklen S, Coulson AR (1977) DNA-sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Schneuwly S, Klemenz R, Gehring WJ (1987) Redesigning the body plan of Drosophila by ectopic expression of the homeotic gene Antennapedia. Nature 325:816–818
Schuh R, Aicher W, Gaul U, Cote S, Preiss A, Maier D, Seifert E, Nauber U, Schröder C, Kemler R, Jäckle H (1986) A conserved family or nuclear proteins containing structural elements of the finger protein encoded by Krüppel, a Drosophila segmentation gene. Cell 47:1025–1032
Sibley MH, Johnson JJ, Mello CC, Kramer JM (1993) Genetic identification, sequence, and alternative splicing of the Caenorhabditis elegans a2(IV) collagen gene. J Cell Biol 123:255–264
Sprenger F, Stevens LM, Nüsslein-Volhard C (1989) The Drosophila gene torso encodes a putative receptor tyrosine kinase. Nature 338:478–483
Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85
Weigel D, Jürgens G, Klingler M, Jäckle H (1990) Two gap genes mediate maternal terminal pattern formation in Drosophila. Science 248:495–498
Zimmermann R, Sagstetter M, Lewis MJ, Pelham HRB (1988) Seventy-kilodalton heat shock proteins and an additional component from reticulocyte lysate stimulate import of M13 procoat protein into microsomes. EMBO J 7:2875–2880
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Reuter, D., Kühnlein, R.P., Frommer, G. et al. Regulation, function and potential origin of the Drosophila gene spalt adjacent, which encodes a secreted protein expressed in the early embryo. Chromosoma 104, 445–454 (1996). https://doi.org/10.1007/BF00352268
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00352268