Abstract
We show that a family of prokaryotic repetitive sequences, called REP (repetitive extragenic palindromic), (Stern et al., 1984) is involved in the formation of chromosomal rearrangements such as duplications. The join-points of seven RecA+ tandem duplications previously characterized in Salmonella typhimurium, that fuse the hisD gene to distant foreign promoters, were cloned and sequenced. In all seven cases they are shown to have originated by recombination between distant REP sequences. Importantly, several join-points had also occurred at REP sequences even in a RecA-background. Thus, REPs can recombine with each other by a RecA(-)-independent mechanism involved in the generation of chromosomal rearrangements. While all RecA+ duplications analysed resulted from recombination between REP sequences, some RecA-duplications did occur also outside of REP sequences, in one case by recombination within a 7 bp homology. Possible roles for the known interaction between DNA gyrase and REP in chromosomal rearrangements are discussed.
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- Albertini A. M., Hofer M., Calos M. P., Miller J. H. On the formation of spontaneous deletions: the importance of short sequence homologies in the generation of large deletions. Cell. 1982 Jun;29(2):319–328. doi: 10.1016/0092-8674(82)90148-9. [DOI] [PubMed] [Google Scholar]
- Anderson P., Roth J. Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. Proc Natl Acad Sci U S A. 1981 May;78(5):3113–3117. doi: 10.1073/pnas.78.5.3113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Anderson R. P., Roth J. R. Tandem chromosomal duplications in Salmonella typhimurium: fusion of histidine genes to novel promoters. J Mol Biol. 1978 Feb 15;119(1):147–166. doi: 10.1016/0022-2836(78)90274-7. [DOI] [PubMed] [Google Scholar]
- Anderson R. P., Roth J. R. Tandem genetic duplications in phage and bacteria. Annu Rev Microbiol. 1977;31:473–505. doi: 10.1146/annurev.mi.31.100177.002353. [DOI] [PubMed] [Google Scholar]
- Bae Y. S., Kawasaki I., Ikeda H., Liu L. F. Illegitimate recombination mediated by calf thymus DNA topoisomerase II in vitro. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2076–2080. doi: 10.1073/pnas.85.7.2076. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown K., Finch P. W., Hickson I. D., Emmerson P. T. Complete nucleotide sequence of the Escherichia coli argA gene. Nucleic Acids Res. 1987 Dec 23;15(24):10586–10586. doi: 10.1093/nar/15.24.10586. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carlomagno M. S., Chiariotti L., Alifano P., Nappo A. G., Bruni C. B. Structure and function of the Salmonella typhimurium and Escherichia coli K-12 histidine operons. J Mol Biol. 1988 Oct 5;203(3):585–606. doi: 10.1016/0022-2836(88)90194-5. [DOI] [PubMed] [Google Scholar]
- Edlund T., Normark S. Recombination between short DNA homologies causes tandem duplication. Nature. 1981 Jul 16;292(5820):269–271. doi: 10.1038/292269a0. [DOI] [PubMed] [Google Scholar]
- Farabaugh P. J., Schmeissner U., Hofer M., Miller J. H. Genetic studies of the lac repressor. VII. On the molecular nature of spontaneous hotspots in the lacI gene of Escherichia coli. J Mol Biol. 1978 Dec 25;126(4):847–857. doi: 10.1016/0022-2836(78)90023-2. [DOI] [PubMed] [Google Scholar]
- Finch P. W., Storey A., Brown K., Hickson I. D., Emmerson P. T. Complete nucleotide sequence of recD, the structural gene for the alpha subunit of Exonuclease V of Escherichia coli. Nucleic Acids Res. 1986 Nov 11;14(21):8583–8594. doi: 10.1093/nar/14.21.8583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finch P. W., Storey A., Chapman K. E., Brown K., Hickson I. D., Emmerson P. T. Complete nucleotide sequence of the Escherichia coli recB gene. Nucleic Acids Res. 1986 Nov 11;14(21):8573–8582. doi: 10.1093/nar/14.21.8573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finch P. W., Wilson R. E., Brown K., Hickson I. D., Tomkinson A. E., Emmerson P. T. Complete nucleotide sequence of the Escherichia coli recC gene and of the thyA-recC intergenic region. Nucleic Acids Res. 1986 Jun 11;14(11):4437–4451. doi: 10.1093/nar/14.11.4437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gasser S. M., Laemmli U. K. Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster. Cell. 1986 Aug 15;46(4):521–530. doi: 10.1016/0092-8674(86)90877-9. [DOI] [PubMed] [Google Scholar]
- Gilson E., Clément J. M., Brutlag D., Hofnung M. A family of dispersed repetitive extragenic palindromic DNA sequences in E. coli. EMBO J. 1984 Jun;3(6):1417–1421. doi: 10.1002/j.1460-2075.1984.tb01986.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilson E., Perrin D., Clement J. M., Szmelcman S., Dassa E., Hofnung M. Palindromic units from E. coli as binding sites for a chromoid-associated protein. FEBS Lett. 1986 Oct 6;206(2):323–328. doi: 10.1016/0014-5793(86)81005-5. [DOI] [PubMed] [Google Scholar]
- Gilson E., Perrin D., Saurin W., Hofnung M. Species specificity of bacterial palindromic units. J Mol Evol. 1987;25(4):371–373. doi: 10.1007/BF02603122. [DOI] [PubMed] [Google Scholar]
- Gilson E., Rousset J. P., Clément J. M., Hofnung M. A subfamily of E. coli palindromic units implicated in transcription termination? Ann Inst Pasteur Microbiol. 1986 Nov-Dec;137B(3):259–270. doi: 10.1016/s0769-2609(86)80116-8. [DOI] [PubMed] [Google Scholar]
- Gyllensten U. B., Erlich H. A. Generation of single-stranded DNA by the polymerase chain reaction and its application to direct sequencing of the HLA-DQA locus. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7652–7656. doi: 10.1073/pnas.85.20.7652. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Higgins C. F., Ames G. F., Barnes W. M., Clement J. M., Hofnung M. A novel intercistronic regulatory element of prokaryotic operons. Nature. 1982 Aug 19;298(5876):760–762. doi: 10.1038/298760a0. [DOI] [PubMed] [Google Scholar]
- Higgins C. F., McLaren R. S., Newbury S. F. Repetitive extragenic palindromic sequences, mRNA stability and gene expression: evolution by gene conversion? A review. Gene. 1988 Dec 10;72(1-2):3–14. doi: 10.1016/0378-1119(88)90122-9. [DOI] [PubMed] [Google Scholar]
- Hill C. W., Grafstrom R. H., Harnish B. W., Hillman B. S. Tandem duplications resulting from recombination between ribosomal RNA genes in Escherichia coli. J Mol Biol. 1977 Nov 5;116(3):407–428. doi: 10.1016/0022-2836(77)90077-8. [DOI] [PubMed] [Google Scholar]
- Hoffman G. R., Walkowicz M. J., Mason J. M., Atkins J. F. Genetic instability associated with the aroC321 allele in Salmonella typhimurium involves genetic duplication. Mol Gen Genet. 1983;190(2):183–188. doi: 10.1007/BF00330638. [DOI] [PubMed] [Google Scholar]
- Lehner A. F., Hill C. W. Involvement of ribosomal ribonucleic acid operons in Salmonella typhimurium chromosomal rearrangements. J Bacteriol. 1980 Jul;143(1):492–498. doi: 10.1128/jb.143.1.492-498.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin R. J., Capage M., Hill C. W. A repetitive DNA sequence, rhs, responsible for duplications within the Escherichia coli K-12 chromosome. J Mol Biol. 1984 Jul 25;177(1):1–18. doi: 10.1016/0022-2836(84)90054-8. [DOI] [PubMed] [Google Scholar]
- Naito A., Naito S., Ikeda H. Homology is not required for recombination mediated by DNA gyrase of Escherichia coli. Mol Gen Genet. 1984;193(2):238–243. doi: 10.1007/BF00330674. [DOI] [PubMed] [Google Scholar]
- Newbury S. F., Smith N. H., Robinson E. C., Hiles I. D., Higgins C. F. Stabilization of translationally active mRNA by prokaryotic REP sequences. Cell. 1987 Jan 30;48(2):297–310. doi: 10.1016/0092-8674(87)90433-8. [DOI] [PubMed] [Google Scholar]
- Nilsson O., Aberg A., Lundqvist T., Sjöberg B. M. Nucleotide sequence of the gene coding for the large subunit of ribonucleotide reductase of Escherichia coli. Correction. Nucleic Acids Res. 1988 May 11;16(9):4174–4174. doi: 10.1093/nar/16.9.4174. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Owen R. J., Borman P. A rapid biochemical method for purifying high molecular weight bacterial chromosomal DNA for restriction enzyme analysis. Nucleic Acids Res. 1987 Apr 24;15(8):3631–3631. doi: 10.1093/nar/15.8.3631. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sadosky A. B., Davidson A., Lin R. J., Hill C. W. rhs gene family of Escherichia coli K-12. J Bacteriol. 1989 Feb;171(2):636–642. doi: 10.1128/jb.171.2.636-642.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, edition VII. Microbiol Rev. 1988 Dec;52(4):485–532. doi: 10.1128/mr.52.4.485-532.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Shyamala V., Ames G. F. Amplification of bacterial genomic DNA by the polymerase chain reaction and direct sequencing after asymmetric amplification: application to the study of periplasmic permeases. J Bacteriol. 1989 Mar;171(3):1602–1608. doi: 10.1128/jb.171.3.1602-1608.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shyamala V., Ames G. F. Genome walking by single-specific-primer polymerase chain reaction: SSP-PCR. Gene. 1989 Dec 7;84(1):1–8. doi: 10.1016/0378-1119(89)90132-7. [DOI] [PubMed] [Google Scholar]
- Smith G. R. Homologous recombination in procaryotes. Microbiol Rev. 1988 Mar;52(1):1–28. doi: 10.1128/mr.52.1.1-28.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sperry A. O., Blasquez V. C., Garrard W. T. Dysfunction of chromosomal loop attachment sites: illegitimate recombination linked to matrix association regions and topoisomerase II. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5497–5501. doi: 10.1073/pnas.86.14.5497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stern M. J., Ames G. F., Smith N. H., Robinson E. C., Higgins C. F. Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell. 1984 Jul;37(3):1015–1026. doi: 10.1016/0092-8674(84)90436-7. [DOI] [PubMed] [Google Scholar]
- Stern M. J., Prossnitz E., Ames G. F. Role of the intercistronic region in post-transcriptional control of gene expression in the histidine transport operon of Salmonella typhimurium: involvement of REP sequences. Mol Microbiol. 1988 Jan;2(1):141–152. doi: 10.1111/j.1365-2958.1988.tb00015.x. [DOI] [PubMed] [Google Scholar]
- Straus D. S., D'Ari Straus L. Large overlapping tandem genetic duplications in Salmonella typhimurium. J Mol Biol. 1976 May 5;103(1):143–153. doi: 10.1016/0022-2836(76)90056-5. [DOI] [PubMed] [Google Scholar]
- Tlsty T. D., Albertini A. M., Miller J. H. Gene amplification in the lac region of E. coli. Cell. 1984 May;37(1):217–224. doi: 10.1016/0092-8674(84)90317-9. [DOI] [PubMed] [Google Scholar]
- Yang Y., Ames G. F. DNA gyrase binds to the family of prokaryotic repetitive extragenic palindromic sequences. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8850–8854. doi: 10.1073/pnas.85.23.8850. [DOI] [PMC free article] [PubMed] [Google Scholar]