Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2001 Feb;157(2):751–764. doi: 10.1093/genetics/157.2.751

Comparative analysis of the nonA region in Drosophila identifies a highly diverged 5' gene that may constrain nonA promoter evolution.

S Campesan 1, D Chalmers 1, F Sandrelli 1, A Megighian 1, A A Peixoto 1, R Costa 1, C P Kyriacou 1
PMCID: PMC1461524  PMID: 11156994

Abstract

A genomic fragment from Drosophila virilis that contained all the no-on-transientA (nonA) coding information, plus several kilobases of upstream material, was identified. Comparisons of nonA sequences and the gene nonA-like in D. melanogaster, a processed duplication of nonA, suggest that it arose before the split between D. melanogaster and D. virilis. In both species, another gene that lies <350 bp upstream from the nonA transcription starts, and that probably corresponds to the lethal gene l(1)i19, was identified. This gene encodes a protein that shows similarities to GPI1, which is required for the biosynthesis of glycosylphosphatidylinositol (GPI), a component for anchoring eukaryotic proteins to membranes, and so we have named it dGpi1. The molecular evolution of nonA and dGpi1 sequences show remarkable differences, with the latter revealing a level of amino acid divergence that is as high as that of transformer and with extremely low levels of codon bias. Nevertheless, in D. melanogaster hosts, the D. virilis fragment rescues the lethality associated with a mutation of l(1)i19e, as well as the viability and visual defects produced by deletion of nonA(-). The presence of dGpi1 sequences so close to nonA appears to have constrained the evolution of the nonA promoter.

Full Text

The Full Text of this article is available as a PDF (830.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bandziulis R. J., Swanson M. S., Dreyfuss G. RNA-binding proteins as developmental regulators. Genes Dev. 1989 Apr;3(4):431–437. doi: 10.1101/gad.3.4.431. [DOI] [PubMed] [Google Scholar]
  2. Bayer C. A., von Kalm L., Fristrom J. W. Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev Biol. 1997 Jul 15;187(2):267–282. doi: 10.1006/dbio.1997.8620. [DOI] [PubMed] [Google Scholar]
  3. Comeron J. M., Kreitman M. The correlation between synonymous and nonsynonymous substitutions in Drosophila: mutation, selection or relaxed constraints? Genetics. 1998 Oct;150(2):767–775. doi: 10.1093/genetics/150.2.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DiBello P. R., Withers D. A., Bayer C. A., Fristrom J. W., Guild G. M. The Drosophila Broad-Complex encodes a family of related proteins containing zinc fingers. Genetics. 1991 Oct;129(2):385–397. doi: 10.1093/genetics/129.2.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Doering T. L., Masterson W. J., Englund P. T., Hart G. W. Biosynthesis of the glycosyl phosphatidylinositol membrane anchor of the trypanosome variant surface glycoprotein. Origin of the non-acetylated glucosamine. J Biol Chem. 1989 Jul 5;264(19):11168–11173. [PubMed] [Google Scholar]
  6. Engelman D. M., Steitz T. A., Goldman A. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Biophys Chem. 1986;15:321–353. doi: 10.1146/annurev.bb.15.060186.001541. [DOI] [PubMed] [Google Scholar]
  7. Englund P. T. The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors. Annu Rev Biochem. 1993;62:121–138. doi: 10.1146/annurev.bi.62.070193.001005. [DOI] [PubMed] [Google Scholar]
  8. Hancock J. M., Armstrong J. S. SIMPLE34: an improved and enhanced implementation for VAX and Sun computers of the SIMPLE algorithm for analysis of clustered repetitive motifs in nucleotide sequences. Comput Appl Biosci. 1994 Feb;10(1):67–70. doi: 10.1093/bioinformatics/10.1.67. [DOI] [PubMed] [Google Scholar]
  9. Hancock J. M., Dover G. A. Molecular coevolution among cryptically simple expansion segments of eukaryotic 26S/28S rRNAs. Mol Biol Evol. 1988 Jul;5(4):377–391. doi: 10.1093/oxfordjournals.molbev.a040505. [DOI] [PubMed] [Google Scholar]
  10. Hancock J. M., Shaw P. J., Bonneton F., Dover G. A. High sequence turnover in the regulatory regions of the developmental gene hunchback in insects. Mol Biol Evol. 1999 Feb;16(2):253–265. doi: 10.1093/oxfordjournals.molbev.a026107. [DOI] [PubMed] [Google Scholar]
  11. Hoikkala A., Lumme J. Genetic control of the difference in male courtship sound between Drosophila virilis and D. lummei. Behav Genet. 1984 May;14(3):257–268. doi: 10.1007/BF01065545. [DOI] [PubMed] [Google Scholar]
  12. Hotta Y., Benzer S. Genetic dissection of the Drosophila nervous system by means of mosaics. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1156–1163. doi: 10.1073/pnas.67.3.1156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jenkins D. L., Ortori C. A., Brookfield J. F. A test for adaptive change in DNA sequences controlling transcription. Proc Biol Sci. 1995 Aug 22;261(1361):203–207. doi: 10.1098/rspb.1995.0137. [DOI] [PubMed] [Google Scholar]
  14. Kanaar R., Roche S. E., Beall E. L., Green M. R., Rio D. C. The conserved pre-mRNA splicing factor U2AF from Drosophila: requirement for viability. Science. 1993 Oct 22;262(5133):569–573. doi: 10.1126/science.7692602. [DOI] [PubMed] [Google Scholar]
  15. Kinoshita T., Inoue N., Takeda J. Defective glycosyl phosphatidylinositol anchor synthesis and paroxysmal nocturnal hemoglobinuria. Adv Immunol. 1995;60:57–103. doi: 10.1016/s0065-2776(08)60584-2. [DOI] [PubMed] [Google Scholar]
  16. Klemenz R., Weber U., Gehring W. J. The white gene as a marker in a new P-element vector for gene transfer in Drosophila. Nucleic Acids Res. 1987 May 26;15(10):3947–3959. doi: 10.1093/nar/15.10.3947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kulkarni S. J., Steinlauf A. F., Hall J. C. The dissonance mutant of courtship song in Drosophila melanogaster: isolation, behavior and cytogenetics. Genetics. 1988 Feb;118(2):267–285. doi: 10.1093/genetics/118.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  19. Leidich S. D., Orlean P. Gpi1, a Saccharomyces cerevisiae protein that participates in the first step in glycosylphosphatidylinositol anchor synthesis. J Biol Chem. 1996 Nov 1;271(44):27829–27837. doi: 10.1074/jbc.271.44.27829. [DOI] [PubMed] [Google Scholar]
  20. Martin C. H., Mayeda C. A., Davis C. A., Ericsson C. L., Knafels J. D., Mathog D. R., Celniker S. E., Lewis E. B., Palazzolo M. J. Complete sequence of the bithorax complex of Drosophila. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8398–8402. doi: 10.1073/pnas.92.18.8398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Connor H. J., Dixon M. F., Wyatt J. I., Axon A. T., Ward D. C., Dewar E. P., Johnston D. Effect of duodenal ulcer surgery and enterogastric reflux on Campylobacter pyloridis. Lancet. 1986 Nov 22;2(8517):1178–1181. doi: 10.1016/s0140-6736(86)92193-8. [DOI] [PubMed] [Google Scholar]
  22. O'Neil M. T., Belote J. M. Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics. 1992 May;131(1):113–128. doi: 10.1093/genetics/131.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pak W. L., Grossfield J., Arnold K. S. Mutants of the visual pathway of Drosophila melanogaster. Nature. 1970 Aug 1;227(5257):518–520. doi: 10.1038/227518b0. [DOI] [PubMed] [Google Scholar]
  24. Peixoto A. A., Campesan S., Costa R., Kyriacou C. P. Molecular evolution of a repetitive region within the per gene of Drosophila. Mol Biol Evol. 1993 Jan;10(1):127–139. doi: 10.1093/oxfordjournals.molbev.a039993. [DOI] [PubMed] [Google Scholar]
  25. Petersen G., Hall J. C., Rosbash M. The period gene of Drosophila carries species-specific behavioral instructions. EMBO J. 1988 Dec 1;7(12):3939–3947. doi: 10.1002/j.1460-2075.1988.tb03280.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Powell J. R., Moriyama E. N. Evolution of codon usage bias in Drosophila. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7784–7790. doi: 10.1073/pnas.94.15.7784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Prestridge D. S. SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput Appl Biosci. 1991 Apr;7(2):203–206. doi: 10.1093/bioinformatics/7.2.203. [DOI] [PubMed] [Google Scholar]
  28. Rendahl K. G., Gaukhshteyn N., Wheeler D. A., Fry T. A., Hall J. C. Defects in courtship and vision caused by amino acid substitutions in a putative RNA-binding protein encoded by the no-on-transient A (nonA) gene of Drosophila. J Neurosci. 1996 Feb 15;16(4):1511–1522. doi: 10.1523/JNEUROSCI.16-04-01511.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rendahl K. G., Jones K. R., Kulkarni S. J., Bagully S. H., Hall J. C. The dissonance mutation at the no-on-transient-A locus of D. melanogaster: genetic control of courtship song and visual behaviors by a protein with putative RNA-binding motifs. J Neurosci. 1992 Feb;12(2):390–407. doi: 10.1523/JNEUROSCI.12-02-00390.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sandrelli F., Campesan S., Rossetto M., Benna C., Zieger E., Megighian A., Couchman M., Kyriacou C., Costa R. Molecular Dissection of the 5' Region of no-on-transientA of Drosophila melanogaster Reveals cis-Regulation by Adjacent dGpi1 Sequences. Genetics. 2001 Feb;157(2):765–775. doi: 10.1093/genetics/157.2.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sandrelli F., Campesan S., Rossetto M., Benna C., Zieger E., Megighian A., Couchman M., Kyriacou C., Costa R. Molecular Dissection of the 5' Region of no-on-transientA of Drosophila melanogaster Reveals cis-Regulation by Adjacent dGpi1 Sequences. Genetics. 2001 Feb;157(2):765–775. doi: 10.1093/genetics/157.2.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sandstrom D. J., Bayer C. A., Fristrom J. W., Restifo L. L. Broad-complex transcription factors regulate thoracic muscle attachment in Drosophila. Dev Biol. 1997 Jan 15;181(2):168–185. doi: 10.1006/dbio.1996.8469. [DOI] [PubMed] [Google Scholar]
  33. Schlötterer C., Hauser M. T., von Haeseler A., Tautz D. Comparative evolutionary analysis of rDNA ITS regions in Drosophila. Mol Biol Evol. 1994 May;11(3):513–522. doi: 10.1093/oxfordjournals.molbev.a040131. [DOI] [PubMed] [Google Scholar]
  34. Sharp P. M., Cowe E., Higgins D. G., Shields D. C., Wolfe K. H., Wright F. Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res. 1988 Sep 12;16(17):8207–8211. doi: 10.1093/nar/16.17.8207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Siomi H., Dreyfuss G. RNA-binding proteins as regulators of gene expression. Curr Opin Genet Dev. 1997 Jun;7(3):345–353. doi: 10.1016/s0959-437x(97)80148-7. [DOI] [PubMed] [Google Scholar]
  36. Spradling A. C., Rubin G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. doi: 10.1126/science.6289435. [DOI] [PubMed] [Google Scholar]
  37. Stanewsky R., Fry T. A., Reim I., Saumweber H., Hall J. C. Bioassaying putative RNA-binding motifs in a protein encoded by a gene that influences courtship and visually mediated behavior in Drosophila: in vitro mutagenesis of nonA. Genetics. 1996 May;143(1):259–275. doi: 10.1093/genetics/143.1.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Stanewsky R., Rendahl K. G., Dill M., Saumweber H. Genetic and molecular analysis of the X chromosomal region 14B17-14C4 in Drosophila melanogaster: loss of function in NONA, a nuclear protein common to many cell types, results in specific physiological and behavioral defects. Genetics. 1993 Oct;135(2):419–442. doi: 10.1093/genetics/135.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tautz D., Tautz C., Webb D., Dover G. A. Evolutionary divergence of promoters and spacers in the rDNA family of four Drosophila species. Implications for molecular coevolution in multigene families. J Mol Biol. 1987 Jun 5;195(3):525–542. doi: 10.1016/0022-2836(87)90181-1. [DOI] [PubMed] [Google Scholar]
  40. Treier M., Pfeifle C., Tautz D. Comparison of the gap segmentation gene hunchback between Drosophila melanogaster and Drosophila virilis reveals novel modes of evolutionary change. EMBO J. 1989 May;8(5):1517–1525. doi: 10.1002/j.1460-2075.1989.tb03536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wheeler D. A., Kyriacou C. P., Greenacre M. L., Yu Q., Rutila J. E., Rosbash M., Hall J. C. Molecular transfer of a species-specific behavior from Drosophila simulans to Drosophila melanogaster. Science. 1991 Mar 1;251(4997):1082–1085. doi: 10.1126/science.1900131. [DOI] [PubMed] [Google Scholar]
  42. von Besser H., Schnabel P., Wieland C., Fritz E., Stanewsky R., Saumweber H. The puff-specific Drosophila protein Bj6, encoded by the gene no-on transient A, shows homology to RNA-binding proteins. Chromosoma. 1990 Dec;100(1):37–47. doi: 10.1007/BF00337601. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES