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Proc Natl Acad Sci U S A. Nov 21, 1995; 92(24): 11095–11099.
PMCID: PMC40578

Restriction-modification systems as genomic parasites in competition for specific sequences.

Abstract

Restriction-modification (RM) systems are believed to have evolved to protect cells from foreign DNA. However, this hypothesis may not be sufficient to explain the diversity and specificity in sequence recognition, as well as other properties, of these systems. We report that the EcoRI restriction endonuclease-modification methylase (rm) gene pair stabilizes plasmids that carry it and that this stabilization is blocked by an RM of the same sequence specificity (EcoRI or its isoschizomer, Rsr I) but not by an RM of a different specificity (PaeR7I) on another plasmid. The PaeR7I rm likewise stabilizes plasmids, unless an rm gene pair with identical sequence specificity is present. Our analysis supports the following model for stabilization and incompatibility: the descendants of cells that have lost an rm gene pair expose the recognition sites in their chromosomes to lethal attack by any remaining restriction enzymes unless modification by another RM system of the same specificity protects these sites. Competition for specific sequences among these selfish genes may have generated the great diversity and specificity in sequence recognition among RM systems. Such altruistic suicide strategies, similar to those found in virus-infected cells, may have allowed selfish RM systems to spread by effectively competing with other selfish genes.

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Selected References

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  • Wilson GG, Murray NE. Restriction and modification systems. Annu Rev Genet. 1991;25:585–627. [PubMed]
  • Korona R, Korona B, Levin BR. Sensitivity of naturally occurring coliphages to type I and type II restriction and modification. J Gen Microbiol. 1993 Jun;139(Pt 6):1283–1290. [PubMed]
  • Bickle TA, Krüger DH. Biology of DNA restriction. Microbiol Rev. 1993 Jun;57(2):434–450. [PMC free article] [PubMed]
  • Levin BR. Frequency-dependent selection in bacterial populations. Philos Trans R Soc Lond B Biol Sci. 1988 Jul 6;319(1196):459–472. [PubMed]
  • Naito T, Kusano K, Kobayashi I. Selfish behavior of restriction-modification systems. Science. 1995 Feb 10;267(5199):897–899. [PubMed]
  • Takahashi NK, Kusano K, Yokochi T, Kitamura Y, Yoshikura H, Kobayashi I. Genetic analysis of double-strand break repair in Escherichia coli. J Bacteriol. 1993 Aug;175(16):5176–5185. [PMC free article] [PubMed]
  • Betlach M, Hershfield V, Chow L, Brown W, Goodman H, Boyer HW. A restriction endonuclease analysis of the bacterial plasmid controlling the ecoRI restriction and modification of DNA. Fed Proc. 1976 Jul;35(9):2037–2043. [PubMed]
  • Gingeras TR, Brooks JE. Cloned restriction/modification system from Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 1983 Jan;80(2):402–406. [PMC free article] [PubMed]
  • Zagursky RJ, Berman ML. Cloning vectors that yield high levels of single-stranded DNA for rapid DNA sequencing. Gene. 1984 Feb;27(2):183–191. [PubMed]
  • Kaszubska W, Aiken C, O'Connor CD, Gumport RI. Purification, cloning and sequence analysis of RsrI DNA methyltransferase: lack of homology between two enzymes, RsrI and EcoRI, that methylate the same nucleotide in identical recognition sequences. Nucleic Acids Res. 1989 Dec 25;17(24):10403–10425. [PMC free article] [PubMed]
  • Summers DK, Sherratt DJ. Multimerization of high copy number plasmids causes instability: CoIE1 encodes a determinant essential for plasmid monomerization and stability. Cell. 1984 Apr;36(4):1097–1103. [PubMed]
  • Stephenson FH, Ballard BT, Boyer HW, Rosenberg JM, Greene PJ. Comparison of the nucleotide and amino acid sequences of the RsrI and EcoRI restriction endonucleases. Gene. 1989 Dec 21;85(1):1–13. [PubMed]
  • Kusano K, Nakayama K, Nakayama H. Plasmid-mediated lethality and plasmid multimer formation in an Escherichia coli recBC sbcBC mutant. Involvement of RecF recombination pathway genes. J Mol Biol. 1989 Oct 20;209(4):623–634. [PubMed]
  • Heitman J, Model P. Site-specific methylases induce the SOS DNA repair response in Escherichia coli. J Bacteriol. 1987 Jul;169(7):3243–3250. [PMC free article] [PubMed]
  • Ogura T, Hiraga S. Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4784–4788. [PMC free article] [PubMed]
  • Gerdes K, Rasmussen PB, Molin S. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc Natl Acad Sci U S A. 1986 May;83(10):3116–3120. [PMC free article] [PubMed]
  • Yarmolinsky MB. Programmed cell death in bacterial populations. Science. 1995 Feb 10;267(5199):836–837. [PubMed]
  • Jacoby GA, Sutton L. Restriction and modification determined by a Pseudomonas R plasmid. Plasmid. 1977 Nov;1(1):115–116. [PubMed]
  • Nordström K, Austin SJ. Mechanisms that contribute to the stable segregation of plasmids. Annu Rev Genet. 1989;23:37–69. [PubMed]
  • Crow JF. The ultraselfish gene. Genetics. 1988 Mar;118(3):389–391. [PMC free article] [PubMed]
  • Beeman RW, Friesen KS, Denell RE. Maternal-effect selfish genes in flour beetles. Science. 1992 Apr 3;256(5053):89–92. [PubMed]
  • Bull JJ, Molineux IJ, Werren JH. Selfish genes. Science. 1992 Apr 3;256(5053):65–65. [PubMed]
  • Peters LL, Barker JE. Novel inheritance of the murine severe combined anemia and thrombocytopenia (Scat) phenotype. Cell. 1993 Jul 16;74(1):135–142. [PubMed]
  • Robbins LG, Pimpinelli S. Chromosome damage and early developmental arrest caused by the Rex element of Drosophila melanogaster. Genetics. 1994 Oct;138(2):401–411. [PMC free article] [PubMed]
  • Wade MJ, Beeman RW. The population dynamics of maternal-effect selfish genes. Genetics. 1994 Dec;138(4):1309–1314. [PMC free article] [PubMed]
  • Vaux DL, Haecker G, Strasser A. An evolutionary perspective on apoptosis. Cell. 1994 Mar 11;76(5):777–779. [PubMed]
  • Hamilton WD. The genetical evolution of social behaviour. I. J Theor Biol. 1964 Jul;7(1):1–16. [PubMed]
  • Yu YT, Snyder L. Translation elongation factor Tu cleaved by a phage-exclusion system. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):802–806. [PMC free article] [PubMed]
  • Parma DH, Snyder M, Sobolevski S, Nawroz M, Brody E, Gold L. The Rex system of bacteriophage lambda: tolerance and altruistic cell death. Genes Dev. 1992 Mar;6(3):497–510. [PubMed]
  • Nölling J, de Vos WM. Characterization of the archaeal, plasmid-encoded type II restriction-modification system MthTI from Methanobacterium thermoformicicum THF: homology to the bacterial NgoPII system from Neisseria gonorrhoeae. J Bacteriol. 1992 Sep;174(17):5719–5726. [PMC free article] [PubMed]
  • Withers BE, Ambroso LA, Dunbar JC. Structure and evolution of the XcyI restriction-modification system. Nucleic Acids Res. 1992 Dec 11;20(23):6267–6273. [PMC free article] [PubMed]
  • Kiss A, Posfai G, Keller CC, Venetianer P, Roberts RJ. Nucleotide sequence of the BsuRI restriction-modification system. Nucleic Acids Res. 1985 Sep 25;13(18):6403–6421. [PMC free article] [PubMed]
  • Raleigh EA, Wilson G. Escherichia coli K-12 restricts DNA containing 5-methylcytosine. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9070–9074. [PMC free article] [PubMed]
  • Barbeyron T, Kean K, Forterre P. DNA adenine methylation of GATC sequences appeared recently in the Escherichia coli lineage. J Bacteriol. 1984 Nov;160(2):586–590. [PMC free article] [PubMed]
  • Kobayashi I. Mechanisms for gene conversion and homologous recombination: the double-strand break repair model and the successive half crossing-over model. Adv Biophys. 1992;28:81–133. [PubMed]
  • Heitman J, Zinder ND, Model P. Repair of the Escherichia coli chromosome after in vivo scission by the EcoRI endonuclease. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2281–2285. [PMC free article] [PubMed]
  • Lambowitz AM, Belfort M. Introns as mobile genetic elements. Annu Rev Biochem. 1993;62:587–622. [PubMed]
  • Gloor GB, Nassif NA, Johnson-Schlitz DM, Preston CR, Engels WR. Targeted gene replacement in Drosophila via P element-induced gap repair. Science. 1991 Sep 6;253(5024):1110–1117. [PubMed]
  • Hagemann AT, Craig NL. Tn7 transposition creates a hotspot for homologous recombination at the transposon donor site. Genetics. 1993 Jan;133(1):9–16. [PMC free article] [PubMed]
  • Hashimoto-Gotoh T, Franklin FC, Nordheim A, Timmis KN. Specific-purpose plasmid cloning vectors. I. Low copy number, temperature-sensitive, mobilization-defective pSC101-derived containment vectors. Gene. 1981 Dec;16(1-3):227–235. [PubMed]

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