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. 1982;1(7):883–888. doi: 10.1002/j.1460-2075.1982.tb01264.x

Constant and variable parts in the Balbiani ring 2 repeat unit and the translation termination region

H Jäckle 1,1, J C de Almeida 1,2, R Galler 1, H Kluding 1, H Lehrach 1, J-E Edström 1,*
PMCID: PMC553126  PMID: 16453423

Abstract

The large Balbiani rings of the chironomids produce giant internally repeated transcripts that are translated into silk-like proteins used for protective tubes. We have cloned fragments of the Balbiani ring 2 (BR2) gene of Chironomus pallidivittatus, normally the most prominent BR, for sequencing and restriction analysis. The results indicate a basic, tandemly arranged repeat unit of 198 bp, consisting of an invariant region of 102 bp followed by a variable region of 96 bp, the latter containing short internal tandem repeats. In the coding strand of both regions, there is a tendency to maximize adenine (˜40%) and minimize cytosine + thymidine (32-33%). Stringency in codon usage and absence of preference for third position nucleotide substitutions between homologous sequences suggest selection at the nucleotide level to be important. Both regions code for peptides rich in basic amino acids, but show distinct differences in other coding properties. The invariant region probably codes for a crystalline domain, and the variable region for a proline-rich, amorphous domain. One of the clones includes the 3' end of the translated region. Surrounding and following two stop codons is a sequence of four short palindromes. Furthermore, the first stop codon is part of a sequence reminiscent of a “TATA box”. The possibilities are discussed that this area of the gene might be a target for regulatory molecules controlling translation termination and/or the expression of an overlapping cistron.

Keywords: Balbiani ring 2, Chironomus, evolution, tandem repeats, palindsomes

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Selected References

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

  1. BEERMANN W. [A Balbiani ring as locus of a salivary gland mutation]. Chromosoma. 1961;12:1–25. doi: 10.1007/BF00328911. [DOI] [PubMed] [Google Scholar]
  2. Beermann W. Directed changes in the pattern of Balbiani ring puffing in Chironomus: effects of a sugar treatment. Chromosoma. 1973;41(3):297–326. doi: 10.1007/BF00344024. [DOI] [PubMed] [Google Scholar]
  3. Bonner J. J., Pardue M. L. Ecdysone-stimulated RNA synthesis in imaginal discs of Drosophila melanogaster. Assay by in situ hybridization. Chromosoma. 1976 Oct 12;58(1):87–99. doi: 10.1007/BF00293443. [DOI] [PubMed] [Google Scholar]
  4. Busslinger M., Portmann R., Birnsteil M. L. A regulatory sequence near the 3' end of sea urchin histone genes. Nucleic Acids Res. 1979 Jul 11;6(9):2997–3008. doi: 10.1093/nar/6.9.2997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Case S. T., Daneholt B. The size of the transcription unit in Balbiani ring 2 of Chironomus tentans as derived from analysis of the primary transcript and 75 S RNA. J Mol Biol. 1978 Sep 5;124(1):223–241. doi: 10.1016/0022-2836(78)90157-2. [DOI] [PubMed] [Google Scholar]
  6. Chavancy G., Garel J. P., Daillie J. Functional adaptation of aminoacyl-tRNA synthetases to fibroin biosynthesis in the silkgland of Bombyx mori L. FEBS Lett. 1975 Jan 1;49(3):380–384. doi: 10.1016/0014-5793(75)80790-3. [DOI] [PubMed] [Google Scholar]
  7. Clewell D. B., Helinski D. R. Supercoiled circular DNA-protein complex in Escherichia coli: purification and induced conversion to an opern circular DNA form. Proc Natl Acad Sci U S A. 1969 Apr;62(4):1159–1166. doi: 10.1073/pnas.62.4.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Daneholt B., Anderson K., Fagerlind M. Large-sized polysomes in Chironomus tentans salivary glands and their relation to Balbiani ring 75S RNA. J Cell Biol. 1977 Apr;73(1):149–160. doi: 10.1083/jcb.73.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Daneholt B. Giant RNA transcript in a Balbiani ring. Nat New Biol. 1972 Dec 20;240(103):229–232. doi: 10.1038/newbio240229a0. [DOI] [PubMed] [Google Scholar]
  10. Degelmann A., Hollenberg C. P. A structural analysis of Balbiani ring dna sequences in Chironomus tentans. Chromosoma. 1981;83(3):295–313. doi: 10.1007/BF00327354. [DOI] [PubMed] [Google Scholar]
  11. Edström J. E., Rydlander L., Francke C. Concomitant induction of a Balbiani ring and a giant secretory protein in Chironomus salivary glands. Chromosoma. 1980;81(1):115–124. doi: 10.1007/BF00292426. [DOI] [PubMed] [Google Scholar]
  12. Francke C., Edström J. E., McDowall A. W., Miller O. L. Electron microscopic visualization of a discrete class of giant translation units in salivary gland cells of Chironomus tentans. EMBO J. 1982;1(1):59–62. doi: 10.1002/j.1460-2075.1982.tb01124.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gage L. P., Manning R. F. Internal structure of the silk fibroin gene of Bombyx mori. I The fibroin gene consists of a homogeneous alternating array of repetitious crystalline and amorphous coding sequences. J Biol Chem. 1980 Oct 10;255(19):9444–9450. [PubMed] [Google Scholar]
  14. Garel J. Quantitative adaptation of isoacceptor tRNAs to mRNA codons of alanine, glycine and serine. Nature. 1976 Apr 29;260(5554):805–806. doi: 10.1038/260805a0. [DOI] [PubMed] [Google Scholar]
  15. Grantham R., Gautier C., Gouy M., Mercier R., Pavé A. Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 1980 Jan 11;8(1):r49–r62. doi: 10.1093/nar/8.1.197-c. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grossbach U. Chromosomen-Aktivitat und biochemische Zelldifferenzierung in den Speicheldrüsen von Camptochironomus. Chromosoma. 1969;28(2):136–187. doi: 10.1007/BF00331528. [DOI] [PubMed] [Google Scholar]
  17. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hollenberg C. P. Proportionate representation of rDNA and Balbiani ring DNA in polytene chromosomes of Chironomus tentans. Chromosoma. 1976 Aug 17;57(2):185–197. doi: 10.1007/BF00292917. [DOI] [PubMed] [Google Scholar]
  19. Honjo T., Obata M., Yamawaki-Katoaka Y., Kataoka T., Kawakami T., Takahashi N., Mano Y. Cloning and complete nucleotide sequence of mouse immunoglobulin gamma 1 chain gene. Cell. 1979 Oct;18(2):559–568. doi: 10.1016/0092-8674(79)90072-2. [DOI] [PubMed] [Google Scholar]
  20. Lambert B. Repeated DNA sequences in a Balbiani ring. J Mol Biol. 1972 Dec 14;72(1):65–75. doi: 10.1016/0022-2836(72)90068-x. [DOI] [PubMed] [Google Scholar]
  21. Lomedico P., Rosenthal N., Efstratidadis A., Gilbert W., Kolodner R., Tizard R. The structure and evolution of the two nonallelic rat preproinsulin genes. Cell. 1979 Oct;18(2):545–558. doi: 10.1016/0092-8674(79)90071-0. [DOI] [PubMed] [Google Scholar]
  22. Maizel J. V., Jr, Lenk R. P. Enhanced graphic matrix analysis of nucleic acid and protein sequences. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7665–7669. doi: 10.1073/pnas.78.12.7665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Majima R., Kawakami M., Shimura K. The biosynthesis of transfer RNA in insects. I. Increase of amino acid acceptor activity of specific tRNA's utilized for silk protein biosynthesis in the silk gland of Bombyx mori. J Biochem. 1975 Aug;78(2):391–400. doi: 10.1093/oxfordjournals.jbchem.a130919. [DOI] [PubMed] [Google Scholar]
  24. Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [DOI] [PubMed] [Google Scholar]
  25. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  26. Olins A. L., Olins D. E., Franke W. W. Stereo-electron microscopy of nucleoli, Balbiani rings and endoplasmic reticulum in Chironomus salivary gland cells. Eur J Cell Biol. 1980 Oct;22(2):714–723. [PubMed] [Google Scholar]
  27. Rydlander L., Edström J. E. Large sized nascent protein as dominating component during protein synthesis in Chironomus salivary glands. Chromosoma. 1980;81(1):85–99. doi: 10.1007/BF00292424. [DOI] [PubMed] [Google Scholar]
  28. Rydlander L., Pigon A., Edström J. E. Sequences translated by Balbiani ring 75S RNA in vitro are present in giant secretory protein from Chironomus tentans. Chromosoma. 1980;81(1):101–113. doi: 10.1007/BF00292425. [DOI] [PubMed] [Google Scholar]
  29. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  30. Tsujimoto Y., Suzuki Y. The DNA sequence of Bombyx mori fibroin gene including the 5' flanking, mRNA coding, entire intervening and fibroin protein coding regions. Cell. 1979 Oct;18(2):591–600. doi: 10.1016/0092-8674(79)90075-8. [DOI] [PubMed] [Google Scholar]
  31. Wieslander L. Number and structure of Balbiani ring 75 S RNA transcription units in Chironomus tentans. J Mol Biol. 1979 Oct 25;134(2):347–367. doi: 10.1016/0022-2836(79)90039-1. [DOI] [PubMed] [Google Scholar]
  32. Wobus U., Bäumlein H., Panitz R., Serfling E., Kafatos F. C. Periodicities and tandem repeats in a Balbiani ring gene. Cell. 1980 Nov;22(1 Pt 1):127–135. doi: 10.1016/0092-8674(80)90161-0. [DOI] [PubMed] [Google Scholar]
  33. Wobus U., Serfling E. The repetition frequency of DNA in Balbiani ring 2 of Chironomus thummi. Chromosoma. 1977 Nov 30;64(3):279–286. doi: 10.1007/BF00328082. [DOI] [PubMed] [Google Scholar]

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