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. 1996 Sep;144(1):171–182. doi: 10.1093/genetics/144.1.171

Comparison of the Structure and Expression of Odd-Skipped and Two Related Genes That Encode a New Family of Zinc Finger Proteins in Drosophila

M C Hart 1, L Wang 1, D E Coulter 1
PMCID: PMC1207491  PMID: 8878683

Abstract

The odd-skipped (odd) gene, which was identified on the basis of a pair-rule segmentation phenotype in mutant embryos, is initially expressed in the Drosophila embryo in seven pair-rule stripes, but later exhibits a segment polarity-like pattern for which no phenotypic correlate is apparent. We have molecularly characterized two embryonically expressed odd-cognate genes, sob and bowel (bowl), that encode proteins with highly conserved C(2)H(2) zinc fingers. While the Sob and Bowl proteins each contain five tandem fingers, the Odd protein lacks a fifth (C-terminal) finger and is also less conserved among the four common fingers. Reminiscent of many segmentation gene paralogues, the closely linked odd and sob genes are expressed during embryogenesis in similar striped patterns; in contrast, the less-tightly linked bowl gene is expressed in a distinctly different pattern at the termini of the early embryo. Although our results indicate that odd and sob are more likely than bowl to share overlapping developmental roles, some functional divergence between the Odd and Sob proteins is suggested by the absence of homology outside the zinc fingers, and also by amino acid substitutions in the Odd zinc fingers at positions that appear to be constrained in Sob and Bowl.

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Selected References

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

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Baumgartner S., Bopp D., Burri M., Noll M. Structure of two genes at the gooseberry locus related to the paired gene and their spatial expression during Drosophila embryogenesis. Genes Dev. 1987 Dec;1(10):1247–1267. doi: 10.1101/gad.1.10.1247. [DOI] [PubMed] [Google Scholar]
  3. Baumgartner S., Noll M. Network of interactions among pair-rule genes regulating paired expression during primordial segmentation of Drosophila. Mech Dev. 1990 Dec;33(1):1–18. doi: 10.1016/0925-4773(90)90130-e. [DOI] [PubMed] [Google Scholar]
  4. Berg J. M. Zinc finger domains: hypotheses and current knowledge. Annu Rev Biophys Biophys Chem. 1990;19:405–421. doi: 10.1146/annurev.bb.19.060190.002201. [DOI] [PubMed] [Google Scholar]
  5. Cadigan K. M., Grossniklaus U., Gehring W. J. Functional redundancy: the respective roles of the two sloppy paired genes in Drosophila segmentation. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6324–6328. doi: 10.1073/pnas.91.14.6324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987 Feb 25;15(4):1353–1361. doi: 10.1093/nar/15.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cherbas L., Cherbas P. The arthropod initiator: the capsite consensus plays an important role in transcription. Insect Biochem Mol Biol. 1993 Jan;23(1):81–90. doi: 10.1016/0965-1748(93)90085-7. [DOI] [PubMed] [Google Scholar]
  8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  9. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Coleman K. G., Poole S. J., Weir M. P., Soeller W. C., Kornberg T. The invected gene of Drosophila: sequence analysis and expression studies reveal a close kinship to the engrailed gene. Genes Dev. 1987 Mar;1(1):19–28. doi: 10.1101/gad.1.1.19. [DOI] [PubMed] [Google Scholar]
  11. Coulter D. E., Swaykus E. A., Beran-Koehn M. A., Goldberg D., Wieschaus E., Schedl P. Molecular analysis of odd-skipped, a zinc finger encoding segmentation gene with a novel pair-rule expression pattern. EMBO J. 1990 Nov;9(11):3795–3804. doi: 10.1002/j.1460-2075.1990.tb07593.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Coulter D. E., Wieschaus E. Gene activities and segmental patterning in Drosophila: analysis of odd-skipped and pair-rule double mutants. Genes Dev. 1988 Dec;2(12B):1812–1823. doi: 10.1101/gad.2.12b.1812. [DOI] [PubMed] [Google Scholar]
  13. DiNardo S., Kuner J. M., Theis J., O'Farrell P. H. Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell. 1985 Nov;43(1):59–69. doi: 10.1016/0092-8674(85)90012-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Forget B. G. Structure and organization of the human globin genes. Tex Rep Biol Med. 1980;40:77–86. [PubMed] [Google Scholar]
  15. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. González-Gaitán M., Rothe M., Wimmer E. A., Taubert H., Jäckle H. Redundant functions of the genes knirps and knirps-related for the establishment of anterior Drosophila head structures. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8567–8571. doi: 10.1073/pnas.91.18.8567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grossniklaus U., Pearson R. K., Gehring W. J. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev. 1992 Jun;6(6):1030–1051. doi: 10.1101/gad.6.6.1030. [DOI] [PubMed] [Google Scholar]
  18. Gutjahr T., Patel N. H., Li X., Goodman C. S., Noll M. Analysis of the gooseberry locus in Drosophila embryos: gooseberry determines the cuticular pattern and activates gooseberry neuro. Development. 1993 May;118(1):21–31. doi: 10.1242/dev.118.1.21. [DOI] [PubMed] [Google Scholar]
  19. Kalderon D., Rubin G. M. cGMP-dependent protein kinase genes in Drosophila. J Biol Chem. 1989 Jun 25;264(18):10738–10748. [PubMed] [Google Scholar]
  20. Li X., Noll M. Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions. Nature. 1994 Jan 6;367(6458):83–87. doi: 10.1038/367083a0. [DOI] [PubMed] [Google Scholar]
  21. Miller J., McLachlan A. D., Klug A. Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 1985 Jun;4(6):1609–1614. doi: 10.1002/j.1460-2075.1985.tb03825.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mullen J. R., DiNardo S. Establishing parasegments in Drosophila embryos: roles of the odd-skipped and naked genes. Dev Biol. 1995 May;169(1):295–308. doi: 10.1006/dbio.1995.1145. [DOI] [PubMed] [Google Scholar]
  23. Nardelli J., Gibson T. J., Vesque C., Charnay P. Base sequence discrimination by zinc-finger DNA-binding domains. Nature. 1991 Jan 10;349(6305):175–178. doi: 10.1038/349175a0. [DOI] [PubMed] [Google Scholar]
  24. Nüsslein-Volhard C., Kluding H., Jürgens G. Genes affecting the segmental subdivision of the Drosophila embryo. Cold Spring Harb Symp Quant Biol. 1985;50:145–154. doi: 10.1101/sqb.1985.050.01.020. [DOI] [PubMed] [Google Scholar]
  25. Patel N. H., Martin-Blanco E., Coleman K. G., Poole S. J., Ellis M. C., Kornberg T. B., Goodman C. S. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell. 1989 Sep 8;58(5):955–968. doi: 10.1016/0092-8674(89)90947-1. [DOI] [PubMed] [Google Scholar]
  26. Pavletich N. P., Pabo C. O. Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science. 1993 Sep 24;261(5129):1701–1707. doi: 10.1126/science.8378770. [DOI] [PubMed] [Google Scholar]
  27. Poole S. J., Kauvar L. M., Drees B., Kornberg T. The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell. 1985 Jan;40(1):37–43. doi: 10.1016/0092-8674(85)90306-x. [DOI] [PubMed] [Google Scholar]
  28. Rosenfeld R., Margalit H. Zinc fingers: conserved properties that can distinguish between spurious and actual DNA-binding motifs. J Biomol Struct Dyn. 1993 Dec;11(3):557–570. doi: 10.1080/07391102.1993.10508015. [DOI] [PubMed] [Google Scholar]
  29. Rothe M., Pehl M., Taubert H., Jäckle H. Loss of gene function through rapid mitotic cycles in the Drosophila embryo. Nature. 1992 Sep 10;359(6391):156–159. doi: 10.1038/359156a0. [DOI] [PubMed] [Google Scholar]
  30. Rothe M., Wimmer E. A., Pankratz M. J., González-Gaitán M., Jäckle H. Identical transacting factor requirement for knirps and knirps-related Gene expression in the anterior but not in the posterior region of the Drosophila embryo. Mech Dev. 1994 Jun;46(3):169–181. doi: 10.1016/0925-4773(94)90069-8. [DOI] [PubMed] [Google Scholar]
  31. Ruddle F. H., Bartels J. L., Bentley K. L., Kappen C., Murtha M. T., Pendleton J. W. Evolution of Hox genes. Annu Rev Genet. 1994;28:423–442. doi: 10.1146/annurev.ge.28.120194.002231. [DOI] [PubMed] [Google Scholar]
  32. Simmonds A. J., Brook W. J., Cohen S. M., Bell J. B. Distinguishable functions for engrailed and invected in anterior-posterior patterning in the Drosophila wing. Nature. 1995 Aug 3;376(6539):424–427. doi: 10.1038/376424a0. [DOI] [PubMed] [Google Scholar]
  33. Smoller D. A., Petrov D., Hartl D. L. Characterization of bacteriophage P1 library containing inserts of Drosophila DNA of 75-100 kilobase pairs. Chromosoma. 1991 Sep;100(8):487–494. doi: 10.1007/BF00352199. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Wang L., Coulter D. E. bowel, an odd-skipped homolog, functions in the terminal pathway during Drosophila embryogenesis. EMBO J. 1996 Jun 17;15(12):3182–3196. [PMC free article] [PubMed] [Google Scholar]
  36. Weir M. P., Kornberg T. Patterns of engrailed and fushi tarazu transcripts reveal novel intermediate stages in Drosophila segmentation. Nature. 1985 Dec 5;318(6045):433–439. doi: 10.1038/318433a0. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Zhang Y., Ungar A., Fresquez C., Holmgren R. Ectopic expression of either the Drosophila gooseberry-distal or proximal gene causes alterations of cell fate in the epidermis and central nervous system. Development. 1994 May;120(5):1151–1161. doi: 10.1242/dev.120.5.1151. [DOI] [PubMed] [Google Scholar]

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