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Stable propagation of ‘selfish’ genetic elements

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Abstract

Extrachromosomal or chromosomally integrated genetic elements are common among prokaryotic and eukaryotic cells. These elements exhibit a variety of ‘selfish’ strategies to ensure their replication and propagation during the growth of their host cells. To establish long-term persistence, they have to moderate the degree of selfishness so as not to imperil the fitness of their hosts. Earlier genetic and biochemical studies together with more recent cell biological investigations have revealed details of the partitioning mechanisms employed by low copy bacterial plasmids. At least some bacterial chromosomes also appear to rely on similar mechanisms for their own segregation. The 2 μm plasmid ofSaccharomyces cerevisiae and related yeast plasmids provide models for optimized eukaryotic selfish DNA elements. Selfish DNA elements exploit the genetic endowments of their hosts without imposing an undue metabolic burden on them. The partitioning systems of these plasmids appear to make use of a molecular trick by which the plasmids feed into the segregation pathway established for the host chromosomes.

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References

  • Barre F-X and Sherratt D J 2002 Xer site-specific recombination: promoting chromosome segregation; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 149–161

    Chapter  Google Scholar 

  • Belfort M, Derbyshire V, Parker M M, Cousineau B and Lam-bowitz A M 2002 Mobile introns: pathways and proteins; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 761–783

    Chapter  Google Scholar 

  • Blat Y and Kleckner N 1999 Cohesins bind to preferential sites along yeast chromosome III with differential regulation along arms versus the centric region;Cell 98 249–259

    Article  CAS  Google Scholar 

  • Bork P, Sander C and Valencia A 1992 An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins;Proc. Natl. Acad. Sci. USA 89 7290–7294

    Article  CAS  Google Scholar 

  • Bouet J Y and Funnell B E 1999 P1 ParA interacts with the P1 partition complex at parS and an ATP-ADP switch controls ParA activities;EMBO J. 18 1415–1424

    Article  CAS  Google Scholar 

  • Carson D R and Christman M F 2001 Evidence that replication fork components catalyze establishment of cohesion between sister chromatids;Proc. Natl. Acad. Sci. USA 98 8270–8275

    Article  CAS  Google Scholar 

  • Cohen-Fix O 2001 The making and breaking of sister chromatid cohesion;Cell 106 137–140

    Article  CAS  Google Scholar 

  • Dawkins R 1992The selfish gene (London: Oxford University Press)

    Google Scholar 

  • Eickbush T H 2002 R2 and related site-specific non-longterminal repeat retrotransposons; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 813–835

    Chapter  Google Scholar 

  • Eliasson A, Bernander R, Dasgupta S and Nordstrom K 1992 Direct visualization of plasmid DNA in bacterial cells;Mol. Microbiol. 6 165–170

    Article  CAS  Google Scholar 

  • Engelberg-Kulka H and Glaser G 1999 Addiction modules and programmed cell death and antideath in bacterial cultures;Annu. Rev. Microbiol. 53 43–70

    Article  CAS  Google Scholar 

  • Engelman E H 2003 Actin’s prokaryotic homologs;Curr. Opin. Struct. Biol. 13 244–248

    Article  Google Scholar 

  • Fedroff N 2002 Control of mobile DNA; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 997–1007

    Chapter  Google Scholar 

  • Futcher A B 1986 Copy number amplification of the 2 micron circle plasmid ofSaccharomyces cerevisiae;J. Theor. Biol. 119 197–204

    Article  CAS  Google Scholar 

  • Gerdes K, Gultyaev A P, Franch T, Pedersen K and Mikkelsen N D 1997 Antisense RNA-regulated programmed cell death;Ann. Rev. Genet. 31 1–31

    Article  CAS  Google Scholar 

  • Gerdes K, Moller-Jensen J and Bugge Jensen R 2000 Plasmid and chromosome partitioning: surprises from phylogeny;Mol. Microbiol. 37 455–466

    Article  CAS  Google Scholar 

  • Hadfield C, Mount R C and Cashmore A M 1995 Protein binding interactions at theSTB locus of the yeast 2 micron plasmid;Nucleic Acids Res. 23 995–1002

    Article  CAS  Google Scholar 

  • Harris A, Young B D and Griffin B E 1985 Random association of Epstein-Barr virus genomes with host cell metaphase chromosomes in Burkitt’s lymphoma-derived cell lines;J. Virol. 56 328–332

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hartl D L, Dykhuizen D E and Berg D E 1984 Accessory DNAs in the bacterial gene pool: playground for coevolution;Ciba Found. Symp. 102 233–245

    CAS  PubMed  Google Scholar 

  • Ilves I, Kivi S and Ustav M 1999 Long-term episomal maintenance of bovine papillomavirus type 1 plasmids is determined by attachment to host chromosomes which is mediated by the viral E2 protein and its binding sites;J. Virol. 73 4404–4412

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ireton K, Gunther N W T and Grossman A D 1994 spo0J is required for normal chromosome segregation as well as the initiation of sporulation inBacillus subtilis;J. Bacteriol. 176 5320–5329

    Article  CAS  Google Scholar 

  • Jensen R B, Lurz R and Gerdes K 1998 Mechanism of DNA segregation in prokaryotes: replicon pairing byparC of plasmid R1;Proc. Natl. Acad. Sci. USA 95 8550–8555

    Article  CAS  Google Scholar 

  • Jones L J, Carballido-Lopez R and Errington J 2001 Control of cell shape in bacteria: helical actin-like filaments inBacillus subtilis;Cell 104 913–922

    Article  CAS  Google Scholar 

  • Kanda T, Otter M and Wahl G M 2001 Coupling of mitotic chromosome tethering and replication competence in Epstein-Barr virus-based plasmids;Mol. Cell Biol. 21 3576–3588

    Article  CAS  Google Scholar 

  • Kobayashi I 2001 Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution;Nucleic Acids Res. 29 3742–3756

    Article  CAS  Google Scholar 

  • Koonin E V 1993a A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication;Nucleic Acids Res. 21 2541–2547

    Article  CAS  Google Scholar 

  • Koonin E V 1993b A superfamily of ATPases with diverse functions containing either classical or deviant ATP-binding motif;J. Mol. Biol. 229 1165–1174

    Article  CAS  Google Scholar 

  • Lehman C W and Botchan M R 1998 Segregation of viral plasmids depends on tethering to chromosomes and is regulated by phosphorylation;Proc. Natl. Acad. Sci. USA 95 4338–4343

    Article  CAS  Google Scholar 

  • Lin D C and Grossman A D 1998 Identification and characterization of a bacterial chromosome partitioning site;Cell 92 675–685

    Article  CAS  Google Scholar 

  • Mehta S, Yang X M, Chan C S, Dobson M J, Jayaram M and Velmurugan S 2002 The 2 micron plasmid purloins the yeast cohesin complex: a mechanism for coupling plasmid partitioning and chromosome segregation?;J. Cell Biol. 158 625–637

    Article  CAS  Google Scholar 

  • Mizuuchi K and Baker T 2002 Chemical mechanisms for mobilizing DNA; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 12–23

    Chapter  Google Scholar 

  • Mohl D A and Gober J W 1997 Cell cycle-dependent polar localization of chromosome partitioning proteins inCaulobacter crescentus;Cell 88 675–684

    CAS  PubMed  Google Scholar 

  • Moller-Jensen J, Jensen R B and Gerdes K 2000 Plasmid and chromosome segregation in prokaryotes;Trends Microbiol. 8 313–320

    Article  CAS  Google Scholar 

  • Moller-Jensen J, Jensen R B, Lowe J and Gerdes K 2002 Prokaryotic DNA segregation by an actin-like filament;EMBO J. 21 3119–3127

    Article  CAS  Google Scholar 

  • Naito T, Kusano K and Kobayashi I 1995 Selfish behaviour of restriction-modification systems;Science 267 897–899

    Article  CAS  Google Scholar 

  • Nasmyth K 2001 Disseminating the genome: joining resolving and separating sister chromatids during mitosis and meiosis;Ann. Rev. Genet. 35 673–745

    Article  CAS  Google Scholar 

  • Nasmyth K, Peters J M and Uhlmann F 2000 Splitting the chromosome: cutting the ties that bind sister chromatids;Science 288 1379–1385

    Article  CAS  Google Scholar 

  • Onogi T, Miki T and Hiraga S 2002 Behavior of sister copies of mini-F plasmid after synchronized plasmid replication inEscherichia coli cells;J. Bacteriol. 184 3142–3145

    Article  CAS  Google Scholar 

  • Plasterk R H and van Luenen H G A M 2002 The Tc1/mariner family of transposable elements; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 519–532

    Chapter  Google Scholar 

  • Pogliano J 2002 Dynamic cellular location of bacterial plasmids;Curr. Opin. Microbiol. 5 586–590

    Article  CAS  Google Scholar 

  • Pogliano J, Ho T Q, Zhong Z and Helinski D R 2001 Multicopy plasmids are clustered and localized inEscherichia coli;Proc. Natl. Acad. Sci. USA 98 4486–4491

    Article  CAS  Google Scholar 

  • Reich Z, Wachtel E J and Minsky A 1994 Liquid-crystalline mesophases of plasmid DNA in bacteria;Science 264 1460–1463

    Article  CAS  Google Scholar 

  • Rio D C 2002 P transposable elements inDrosophila melanogaster; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 484–518

    Chapter  Google Scholar 

  • Sandmeyer S B, Aye M and Menees T 2002 Ty3, a position specific, Gypsy-like element inSaccharomyces cerevisiae; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 663–683

    Chapter  Google Scholar 

  • Scott-Drew S and Murray J A 1998 Localisation and interaction of the protein components of the yeast 2 micron circle plasmid partitioning system suggest a mechanism for plasmid inheritance;J. Cell Sci. 111 1779–1789

    CAS  PubMed  Google Scholar 

  • Scott-Drew S, Wong C M and Murray J A 2002 DNA plasmid transmission in yeast is associated with specific sub-nuclear localization during cell division;Cell Biol. Int. 26 393–405

    Article  CAS  Google Scholar 

  • Sengupta A, Blomqvist K, Pickett A J, Zhang Y, Chew J S and Dobson M J 2001 Functional domains of yeast plasmidencoded Rep proteins;J. Bacteriol. 183 2306–2315

    Article  CAS  Google Scholar 

  • Skibbens R V, Corson L B, Koshland D and Hieter P 1999 Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery;Genes Dev. 13 307–319

    Article  CAS  Google Scholar 

  • Som T, Armstrong K A, Volkert F C and Broach J R 1988 Autoregulation of 2 micron circle gene expression provides a model for maintenance of stable plasmid copy levels;Cell 52 27–37

    Article  CAS  Google Scholar 

  • Stephens C 2002 Chromosome segregation: pushing plasmids apart;Curr. Biol. 12 728–730

    Article  Google Scholar 

  • Sunako Y, Onogi T and Hiraga S 2001 Sister chromosome cohesion ofEscherichia coli;Mol. Microbiol. 42 1233–1241

    Article  CAS  Google Scholar 

  • Sundstrom L and Boomsma J J 2001 Conflicts and alliances in insect families;Heredity 86 515–521

    Article  CAS  Google Scholar 

  • Tanaka T, Cosma M P, Wirth K and Nasmyth K 1999 Identification of cohesin association sites at centromeres and along chromosome arms;Cell 98 847–858

    Article  CAS  Google Scholar 

  • Thomas C M 2000 Paradigms of plasmid organization;Mol. Microbiol. 37 485–491

    Article  CAS  Google Scholar 

  • Toth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A and Nasmyth K 1999 Yeast cohesin complex requires a conserved protein Eco1p (Ctf7) to establish cohesion between sister chromatids during DNA replication;Genes Dev. 13 320–333

    Article  CAS  Google Scholar 

  • Uhlmann F, Lottspeich F and Nasmyth K 1999 Sister-chroma-tid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1;Nature (London) 400 37–42

    Article  CAS  Google Scholar 

  • Uhlmann F and Nasmyth K 1998 Cohesion between sister chromatids must be established during DNA replication;Curr. Biol. 8 1095–1101

    Article  CAS  Google Scholar 

  • Uhlmann F, Wernic D, Poupart M A, Koonin E V and Nasmyth K 2000 Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast;Cell 103 375–386

    Article  CAS  Google Scholar 

  • van den Ent F, Amos L and Lowe J 2001a Bacterial ancestry of actin and tubulin;Curr. Opin. Microbiol. 4 634–638

    Article  Google Scholar 

  • van den Ent F, Amos L A and Lowe J 2001b Prokaryotic origin of the actin cytoskeleton;Nature (London) 413 39–44

    Article  Google Scholar 

  • Velmurugan S, Mehta S and Jayaram M 2003 Selfishness in moderation: evolutionary success of the yeast plasmid;Curr. Topics Dev. Biol. 56 (in press)

  • Velmurugan S, Yang X M, Chan C S, Dobson M and Jayaram M 2000 Partitioning of the 2-micron circle plasmid ofSaccharomyces cerevisiae. Functional coordination with chromosome segregation and plasmid-encoded rep protein distribution;J. Cell Biol. 149 553–566

    Article  CAS  Google Scholar 

  • Yamanaka K T S, Inouye S and Inouye M 2002 Retrons; inMobile DNA II (eds) N L Craig, R Craigie, M Gellert and A M Lambowitz (Washington DC: ASM Press) pp 784–795

    Chapter  Google Scholar 

  • Yates P, Lane D and Biek D P 1999 The F plasmid centromeresopC is required for full repression of the sopAB operon;J. Mol. Biol. 290 627–638

    Article  CAS  Google Scholar 

  • Zechiedrich E L, Khodursky A B, Bachellier S, Schneider R, Chen D, Lilley D M and Cozzarelli N R 2000 Roles of topoisomerases in maintaining steady-state DNA supercoiling inEscherichia coli;J. Biol. Chem. 275 8103–8113

    Article  CAS  Google Scholar 

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  1. Section of Molecular Genetics and Microbiology, University of Texas at Austin, 78712, Austin, TX, USA

    Soundarapandian Velmurugan, Shwetal Mehta, Dina Uzri & Makkuni Jayaram

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  1. Soundarapandian Velmurugan
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  2. Shwetal Mehta
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  3. Dina Uzri
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  4. Makkuni Jayaram
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Correspondence to Makkuni Jayaram.

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Velmurugan, S., Mehta, S., Uzri, D. et al. Stable propagation of ‘selfish’ genetic elements. J. Biosci. 28, 623–636 (2003). https://doi.org/10.1007/BF02703338

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