Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Jun 15;90(12):5464–5468. doi: 10.1073/pnas.90.12.5464

Drosophila evolution challenges postulated redundancy in the E(spl) gene complex.

D Maier 1, B M Marte 1, W Schäfer 1, Y Yu 1, A Preiss 1
PMCID: PMC46741  PMID: 8516287

Abstract

The Enhancer of split [E(spl)] gene complex belongs to the class of neurogenic loci, which, in a concerted action, govern neurogenesis in Drosophila. Two genetically distinct functions, vital and neurogenic, reside within the complex defined by lethal mutations in the l(3) gro gene and by the typical neurogenic phenotype of deletions, respectively. Such deletions always affect several of the many embryonically active genes in the region, which cannot be mutated separately to lethality. Seven of these genes are extremely similar at the transcription and sequence level sharing the basic helix-loop-helix (bHLH) motif of transcriptional regulators. While these E(spl) bHLH genes seem to be required collectively for neurogenesis, they are nonessential individually, suggesting functional redundancy of the encoded gene products. No specific functions could yet be ascribed to any of the other genes located within the complex. One might expect these apparently dispensable genes, as well as the supposedly redundant bHLH genes, to be under little evolutionary constraint and, thus, to evolve most rapidly. However, we find the entire E(spl) gene complex highly conserved during Drosophila evolution, indicating that all the genes as well as their organization are of functional importance.

Full text

PDF
5464

Images in this article

5465Fig. 1
on p.5465
5467Fig. 3
on p.5467
5467Fig. 4
on p.5467

Selected References

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

  1. Artavanis-Tsakonas S., Delidakis C., Fehon R. G. The Notch locus and the cell biology of neuroblast segregation. Annu Rev Cell Biol. 1991;7:427–452. doi: 10.1146/annurev.cb.07.110191.002235. [DOI] [PubMed] [Google Scholar]
  2. Artavanis-Tsakonas S., Simpson P. Choosing a cell fate: a view from the Notch locus. Trends Genet. 1991 Nov-Dec;7(11-12):403–408. doi: 10.1016/0168-9525(91)90264-q. [DOI] [PubMed] [Google Scholar]
  3. Beverley S. M., Wilson A. C. Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J Mol Evol. 1984;21(1):1–13. doi: 10.1007/BF02100622. [DOI] [PubMed] [Google Scholar]
  4. Bier E., Vaessin H., Younger-Shepherd S., Jan L. Y., Jan Y. N. deadpan, an essential pan-neural gene in Drosophila, encodes a helix-loop-helix protein similar to the hairy gene product. Genes Dev. 1992 Nov;6(11):2137–2151. doi: 10.1101/gad.6.11.2137. [DOI] [PubMed] [Google Scholar]
  5. Brookfield J. Can genes be truly redundant? Curr Biol. 1992 Oct;2(10):553–554. doi: 10.1016/0960-9822(92)90036-a. [DOI] [PubMed] [Google Scholar]
  6. Caccone A., Powell J. R. Extreme rates and heterogeneity in insect DNA evolution. J Mol Evol. 1990 Mar;30(3):273–280. doi: 10.1007/BF02099997. [DOI] [PubMed] [Google Scholar]
  7. Campos-Ortega J. A., Knust E. Genetics of early neurogenesis in Drosophila melanogaster. Annu Rev Genet. 1990;24:387–407. doi: 10.1146/annurev.ge.24.120190.002131. [DOI] [PubMed] [Google Scholar]
  8. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  9. Delidakis C., Artavanis-Tsakonas S. The Enhancer of split [E(spl)] locus of Drosophila encodes seven independent helix-loop-helix proteins. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8731–8735. doi: 10.1073/pnas.89.18.8731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Delidakis C., Preiss A., Hartley D. A., Artavanis-Tsakonas S. Two genetically and molecularly distinct functions involved in early neurogenesis reside within the Enhancer of split locus of Drosophila melanogaster. Genetics. 1991 Nov;129(3):803–823. doi: 10.1093/genetics/129.3.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Domier L. L., Rivard J. J., Sabatini L. M., Blumenfeld M. Drosophila virilis histone gene clusters lacking H1 coding segments. J Mol Evol. 1986;23(2):149–158. doi: 10.1007/BF02099909. [DOI] [PubMed] [Google Scholar]
  13. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  14. Goodman M., Moore G. W., Matsuda G. Darwinian evolution in the genealogy of haemoglobin. Nature. 1975 Feb 20;253(5493):603–608. doi: 10.1038/253603a0. [DOI] [PubMed] [Google Scholar]
  15. Hartley D. A., Preiss A., Artavanis-Tsakonas S. A deduced gene product from the Drosophila neurogenic locus, enhancer of split, shows homology to mammalian G-protein beta subunit. Cell. 1988 Dec 2;55(5):785–795. doi: 10.1016/0092-8674(88)90134-1. [DOI] [PubMed] [Google Scholar]
  16. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  17. Jukes T. H., King J. L. Evolutionary nucleotide replacements in DNA. Nature. 1979 Oct 18;281(5732):605–606. doi: 10.1038/281605a0. [DOI] [PubMed] [Google Scholar]
  18. Klämbt C., Knust E., Tietze K., Campos-Ortega J. A. Closely related transcripts encoded by the neurogenic gene complex enhancer of split of Drosophila melanogaster. EMBO J. 1989 Jan;8(1):203–210. doi: 10.1002/j.1460-2075.1989.tb03365.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Knust E., Schrons H., Grawe F., Campos-Ortega J. A. Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics. 1992 Oct;132(2):505–518. doi: 10.1093/genetics/132.2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Knust E., Schrons H., Grawe F., Campos-Ortega J. A. Seven genes of the Enhancer of split complex of Drosophila melanogaster encode helix-loop-helix proteins. Genetics. 1992 Oct;132(2):505–518. doi: 10.1093/genetics/132.2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Knust E., Tietze K., Campos-Ortega J. A. Molecular analysis of the neurogenic locus Enhancer of split of Drosophila melanogaster. EMBO J. 1987 Dec 20;6(13):4113–4123. doi: 10.1002/j.1460-2075.1987.tb02757.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Maier D., Preiss A., Powell J. R. Regulation of the segmentation gene fushi tarazu has been functionally conserved in Drosophila. EMBO J. 1990 Dec;9(12):3957–3966. doi: 10.1002/j.1460-2075.1990.tb07616.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maier D., Stumm G., Kuhn K., Preiss A. Hairless, a Drosophila gene involved in neural development, encodes a novel, serine rich protein. Mech Dev. 1992 Aug;38(2):143–156. doi: 10.1016/0925-4773(92)90006-6. [DOI] [PubMed] [Google Scholar]
  24. Murre C., McCaw P. S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell. 1989 Mar 10;56(5):777–783. doi: 10.1016/0092-8674(89)90682-x. [DOI] [PubMed] [Google Scholar]
  25. Preiss A., Hartley D. A., Artavanis-Tsakonas S. The molecular genetics of Enhancer of split, a gene required for embryonic neural development in Drosophila. EMBO J. 1988 Dec 1;7(12):3917–3927. doi: 10.1002/j.1460-2075.1988.tb03278.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rushlow C. A., Hogan A., Pinchin S. M., Howe K. M., Lardelli M., Ish-Horowicz D. The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N-myc. EMBO J. 1989 Oct;8(10):3095–3103. doi: 10.1002/j.1460-2075.1989.tb08461.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Stifani S., Blaumueller C. M., Redhead N. J., Hill R. E., Artavanis-Tsakonas S. Human homologs of a Drosophila Enhancer of split gene product define a novel family of nuclear proteins. Nat Genet. 1992 Oct;2(2):119–127. doi: 10.1038/ng1092-119. [DOI] [PubMed] [Google Scholar]
  29. Tabor S., Richardson C. C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. doi: 10.1073/pnas.84.14.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tautz D., Pfeifle C. 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. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  31. Wharton K. A., Yedvobnick B., Finnerty V. G., Artavanis-Tsakonas S. opa: a novel family of transcribed repeats shared by the Notch locus and other developmentally regulated loci in D. melanogaster. Cell. 1985 Jan;40(1):55–62. doi: 10.1016/0092-8674(85)90308-3. [DOI] [PubMed] [Google Scholar]
  32. Ziemer A., Tietze K., Knust E., Campos-Ortega J. A. Genetic analysis of enhancer of split, a locus involved in neurogenesis in Drosophila melanogaster. Genetics. 1988 May;119(1):63–74. doi: 10.1093/genetics/119.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES