Abstract
A number of genes of the developmental gene hierarchy in Drosophila encode transcription factors containing Cys2His2 zinc finger domains as DNA-binding motifs. To learn more about the evolution of these genes, it is necessary to clone the homologs, or more correctly the orthologs, from different species. Using PCR, we were able to obtain apparently orthologous fragments of hunchback (hb), Krüppel (Kr), and snail (sna) from a variety of arthropods and partly also from other animal phyla. Sequence alignments of these fragments show that the amino acid differences can normally not be correlated with the evolutionary distances of the respective species. This is due to an apparent saturation of potential replacements within the finger domains, which is also evident from the frequent occurrence of convergent replacements. Another recurrent feature of these alignments is that those amino acids that are directly involved in determining the DNA-binding specificity of the fingers are most conserved. Using in vitro bandshift experiments we can indeed show that the binding specificity of a hunchback finger fragment from different species is not changed. This implies that there is a high selective pressure to maintain the regulatory target elements of these genes during evolution.
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- Berg J. M. Proposed structure for the zinc-binding domains from transcription factor IIIA and related proteins. Proc Natl Acad Sci U S A. 1988 Jan;85(1):99–102. doi: 10.1073/pnas.85.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boulay J. L., Dennefeld C., Alberga A. The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. 1987 Nov 26-Dec 2Nature. 330(6146):395–398. doi: 10.1038/330395a0. [DOI] [PubMed] [Google Scholar]
- Brown R. S., Sander C., Argos P. The primary structure of transcription factor TFIIIA has 12 consecutive repeats. FEBS Lett. 1985 Jul 8;186(2):271–274. doi: 10.1016/0014-5793(85)80723-7. [DOI] [PubMed] [Google Scholar]
- Chowdhury K., Deutsch U., Gruss P. A multigene family encoding several "finger" structures is present and differentially active in mammalian genomes. Cell. 1987 Mar 13;48(5):771–778. doi: 10.1016/0092-8674(87)90074-2. [DOI] [PubMed] [Google Scholar]
- Fitch W. M. Distinguishing homologous from analogous proteins. Syst Zool. 1970 Jun;19(2):99–113. [PubMed] [Google Scholar]
- Frankel A. D., Berg J. M., Pabo C. O. Metal-dependent folding of a single zinc finger from transcription factor IIIA. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4841–4845. doi: 10.1073/pnas.84.14.4841. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoch M., Seifert E., Jäckle H. Gene expression mediated by cis-acting sequences of the Krüppel gene in response to the Drosophila morphogens bicoid and hunchback. EMBO J. 1991 Aug;10(8):2267–2278. doi: 10.1002/j.1460-2075.1991.tb07763.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hülskamp M., Pfeifle C., Tautz D. A morphogenetic gradient of hunchback protein organizes the expression of the gap genes Krüppel and knirps in the early Drosophila embryo. Nature. 1990 Aug 9;346(6284):577–580. doi: 10.1038/346577a0. [DOI] [PubMed] [Google Scholar]
- Hülskamp M., Tautz D. Gap genes and gradients--the logic behind the gaps. Bioessays. 1991 Jun;13(6):261–268. doi: 10.1002/bies.950130602. [DOI] [PubMed] [Google Scholar]
- Ingham P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature. 1988 Sep 1;335(6185):25–34. doi: 10.1038/335025a0. [DOI] [PubMed] [Google Scholar]
- Johnson P. F., McKnight S. L. Eukaryotic transcriptional regulatory proteins. Annu Rev Biochem. 1989;58:799–839. doi: 10.1146/annurev.bi.58.070189.004055. [DOI] [PubMed] [Google Scholar]
- Kadonaga J. T., Carner K. R., Masiarz F. R., Tjian R. Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell. 1987 Dec 24;51(6):1079–1090. doi: 10.1016/0092-8674(87)90594-0. [DOI] [PubMed] [Google Scholar]
- Lee M. S., Gippert G. P., Soman K. V., Case D. A., Wright P. E. Three-dimensional solution structure of a single zinc finger DNA-binding domain. Science. 1989 Aug 11;245(4918):635–637. doi: 10.1126/science.2503871. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Pavletich N. P., Pabo C. O. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science. 1991 May 10;252(5007):809–817. doi: 10.1126/science.2028256. [DOI] [PubMed] [Google Scholar]
- Rosenberg A. H., Lade B. N., Chui D. S., Lin S. W., Dunn J. J., Studier F. W. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene. 1987;56(1):125–135. doi: 10.1016/0378-1119(87)90165-x. [DOI] [PubMed] [Google Scholar]
- Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
- Sargent M. G., Bennett M. F. Identification in Xenopus of a structural homologue of the Drosophila gene snail. Development. 1990 Aug;109(4):967–973. doi: 10.1242/dev.109.4.967. [DOI] [PubMed] [Google Scholar]
- Schuh R., Aicher W., Gaul U., Côté S., Preiss A., Maier D., Seifert E., Nauber U., Schröder C., Kemler R. A conserved family of nuclear proteins containing structural elements of the finger protein encoded by Krüppel, a Drosophila segmentation gene. Cell. 1986 Dec 26;47(6):1025–1032. doi: 10.1016/0092-8674(86)90817-2. [DOI] [PubMed] [Google Scholar]
- Sommer R., Tautz D. Minimal homology requirements for PCR primers. Nucleic Acids Res. 1989 Aug 25;17(16):6749–6749. doi: 10.1093/nar/17.16.6749. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sommer R., Tautz D. Segmentation gene expression in the housefly Musca domestica. Development. 1991 Oct;113(2):419–430. doi: 10.1242/dev.113.2.419. [DOI] [PubMed] [Google Scholar]
- Stanojević D., Hoey T., Levine M. Sequence-specific DNA-binding activities of the gap proteins encoded by hunchback and Krüppel in Drosophila. Nature. 1989 Sep 28;341(6240):331–335. doi: 10.1038/341331a0. [DOI] [PubMed] [Google Scholar]
- Thukral S. K., Morrison M. L., Young E. T. Alanine scanning site-directed mutagenesis of the zinc fingers of transcription factor ADR1: residues that contact DNA and that transactivate. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9188–9192. doi: 10.1073/pnas.88.20.9188. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Treisman J., Desplan C. The products of the Drosophila gap genes hunchback and Krüppel bind to the hunchback promoters. Nature. 1989 Sep 28;341(6240):335–337. doi: 10.1038/341335a0. [DOI] [PubMed] [Google Scholar]
- Tso J. Y., Van Den Berg D. J., Korn L. J. Structure of the gene for Xenopus transcription factor TFIIIA. Nucleic Acids Res. 1986 Mar 11;14(5):2187–2200. doi: 10.1093/nar/14.5.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whiteley M., Noguchi P. D., Sensabaugh S. M., Odenwald W. F., Kassis J. A. The Drosophila gene escargot encodes a zinc finger motif found in snail-related genes. Mech Dev. 1992 Feb;36(3):117–127. doi: 10.1016/0925-4773(92)90063-p. [DOI] [PubMed] [Google Scholar]
- el-Baradi T., Pieler T. Zinc finger proteins: what we know and what we would like to know. Mech Dev. 1991 Nov;35(3):155–169. doi: 10.1016/0925-4773(91)90015-x. [DOI] [PubMed] [Google Scholar]