The cost of copy number in a selfish genetic element: The 2-μm plasmid of Saccharomyces cerevisiae

Journal of Evolutionary Biology

Volumn 25, Issue 11, 2012, Pages 2348-2356

  Harrison, E ^a,c   Koufopanou, V ^a   Burt, A ^a   MacLean, R C ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF YORK   (United Kingdom)

Author keywords

2 m; Fitness cost; Multicopy elements; Plasmid evolution; Yeast

Indexed keywords

FUNGAL PROTEIN; GALACTOSE; URACIL;

DISEASE TRANSMISSION; EVOLUTIONARY BIOLOGY; FITNESS; GROWTH RATE; PLASMID; REPRODUCTIVE COST; TRADE-OFF; VIRULENCE; YEAST;

ARTICLE; COPY NUMBER VARIATION; FUNGAL GENE; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PLASMID; SACCHAROMYCES CEREVISIAE;

BASE SEQUENCE; DNA COPY NUMBER VARIATIONS; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GALACTOSE; GENES, FUNGAL; PLASMIDS; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC; URACIL;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 84868154443     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2012.02610.x     Document Type: Article

References (51)

1. Alfieri, J.A. & Clark, D.J. 1999. Isolation of minichromosomes from yeast cells. Chromatin 304: 35-49.
2. Amberg, D., Burke, D. & Strathern, J. 2005. Methods in Yeast Genetics. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NY, USA.
3. Bentley, W.E., Mirjalili, N., Andersen, D.C., Davis, R.H. & Kompala, D.S. 1990. Plasmid-encoded protein - the principal factor in the metabolic burden associated with recombinant bacteria. Biotechnol. Bioeng. 35: 668-681.
4. Bouma, J.E. & Lenski, R.E. 1988. Evolution of a bacteria plasmid association. Nature 335: 351-352.
5. Bull, J.J. 1994. Perspective - virulence. Evolution 48: 1423-1437.
6. Burgess, R.C., Rahman, S., Lisby, M., Rothstein, R. & Zhao, X.L. 2007. The slx5-slx8 complex affects sumoylation of DNA repair proteins and negatively regulates recombination. Mol. Cell. Biol. 27: 6153-6162.
7. Burt, A. & Trivers, R. 2006. Genes in Conflict: The Biology of Selfish Genetic Elements. Belknap Press, Cambridge, MA, USA.
8. Chen, X.L., Reindle, A. & Johnson, E.S. 2005. Misregulation of 2 mu m circle copy number in a SUMO pathway mutant. Mol. Cell. Biol. 25: 4311-4320.
9. Chung, B.H., Kim, S.J., Kang, H.A. & Yu, M.H. 1998. Secretory expression of human alpha(1)-antitrypsin in Saccharomyces cerevisiae using galactose as a gratuitous inducer. Biotechnol. Lett. 20: 307-311.
10. Corchero, J.L. & Villaverde, A. 1998. Plasmid maintenance in Escherichia coli recombinant cultures is dramatically, steadily, and specifically influenced by features of the encoded proteins. Biotechnol. Bioeng. 58: 625-632.
11. Dahlberg, C. & Chao, L. 2003. Amelioration of the cost of conjugative plasmid carriage in Escherichia coli K12. Genetics 165: 1641-1649.
12. Danhash, N., Gardner, D.C.J. & Oliver, S.G. 1991. Heritable damage to yeast caused by transformation. Biotechnology 9: 179-182.
13. Dionisio, F., Conceicao, I.C., Marques, A.C.R., Fernandes, L. & Gordo, I. 2005. The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol. Lett. 1: 250-252.
14. Dobson, M.J., Pickett, A.J., Velmurugan, S., Pinder, J.B., Barrett, L.A., Jayaram, M. et al. 2005. The 2 mu m plasmid causes cell death in Saccharomyces cerevisiae with a mutation in Ulp1 protease. Mol. Cell. Biol. 25: 4299-4310.
15. Eanes, W.F., Wesley, C., Hey, J., Houle, D. & Ajioka, J.W. 1988. The fitness consequences of P-element insertion in Drosophila-melanogaster. Genet. Res. 52: 17-26.
16. Engberg, B., Hjalmarsson, K. & Nordstrom, K. 1975. Inhibition of cell-division in Escherichia-coli K-12 by R-factor R1 and copy mutants of R1. J. Bacteriol. 124: 633-640.
17. Frank, S.A. 1996. Models of parasite virulence. Q. Rev. Biol. 71: 37-78.
18. Futcher, A.B. & Cox, B.S. 1983. Maintenance of the 2μm circle plasmid in populations of Saccharomyces cerevisiae. J. Bacteriol. 154: 612-622.
19. Futcher, A.B. & Cox, B.S. 1984. Copy number and the stability of 2μm circle-based artificial plasmids of Saccharomyces cerevisiae. J. Bacteriol. 157: 283-290.
20. Gerbaud, C. & Guerineau, M. 1980. 2μm plasmid copy number in different yeast strains and repartition of endogenous and 2μm chimeric plasmids in transformed strains. Curr. Genet. 1: 219-228.
21. Hall, B.G., Parker, L.L., Betts, P.W., Dubose, R.F., Sawyer, S.A. & Hartl, D.L. 1989. IS103, a new insertion element in Escherichia coli - characterization and distribution in natural populations. Genetics 121: 423-431.
22. Hartl, D.L. & Clark, A.G. 1997. Principles of Population Genetics, 3rd edn. Sinauer Associates, Sunderland, MA, USA.
23. Holm, C. 1982. Sensitivity to the yeast plasmid 2μm DNA is conferred by the nuclear allele nib-1. Mol. Cell. Biol. 2: 985-992.
24. Hua-Van, A., Le Rouzic, A., Boutin, T.S., Filee, J. & Capy, P. 2011. The struggle for life of the genome's selfish architects. Biol. Direct 6: 19.
25. Johnson, L.J., Koufopanou, V., Goddard, M.R., Hetherington, R., Schafer, S.M. & Burt, A. 2004. Population genetics of the wild yeast Saccharomyces paradoxus. Genetics 166: 43-52.
26. Lee, C., Kim, J., Shin, S.G. & Hwang, S. 2006. Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J. Biotechnol. 123: 273-280.
27. Livak, K.J. & Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
28. MacLean, R.C. 2007. Pleiotropy and GAL pathway degeneration in yeast. J. Evol. Biol. 20: 1333-1338.
29. MacLean, R.C., Perron, G.G. & Gardner, A. 2010. Diminishing returns from beneficial mutations and pervasive epistasis shape the fitness landscape for rifampicin resistance in Pseudomonas aeruginosa. Genetics 186: 1345-1354.
30. Malik, H.S. 2006. A hitchhiker's guide to survival finally makes CENs. J. Cell Biol. 174: 747-749.
31. Mead, D.J., Gardener, D.C.J. & Oliver, S.G. 1986. The yeast 2μm plasmid- strategies for the survival of a selfish DNA. Mol. Gen. Genet. 20: 417-421.
32. Mead, D.J., Gardner, D.C.J. & Oliver, S.G. 1987. Phenotypic differences between induced and spontaneous 2μm-plasmid-free segregants of Saccharomyces cerevisiae. Curr. Genet. 11: 415-418.
33. Min, K.T. & Benzer, S. 1997. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl Acad. Sci. USA 94: 10792-10796.
34. Modi, R.I. & Adams, J. 1991. Coevolution in bacterial - plasmid populations. Evolution 45: 656-667.
35. Mouton, L., Henri, H., Charif, D., Bouletrea, M. & Vavre, F. 2007. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol. Lett. 3: 210-213.
36. Murray, J.A.H., Scarpa, M., Rossi, N. & Cesareni, G. 1987. Antagonistic controls regulate copy number of the yeast 2μm plasmid. EMBO J. 6: 4205-4212.
37. Nakayashiki, T., Kurtzman, C.P., Edskes, H.K. & Wickner, R.B. 2005. Yeast prions [URE3] and [PSI+] are diseases. Proc. Natl Acad. Sci. USA 102: 10575-10580.
38. Pasyukova, E.G., Nuzhdin, S.V., Morozova, T.V. & Mackay, T.F.C. 2004. Accumulation of transposable elements in the genome of Drosophila melanogaster is associated with a decrease in fitness. J. Hered. 95: 284-290.
39. Patnaik, P.R. 2000. An evaluation of models for the effect of plasmid copy number on bacterial growth rate. Biotechnol. Lett. 22: 1719-1725.
40. Paulsson, J. 2002. Multileveled selection on plasmid replication. Genetics 161: 1373-1384.
41. Rankin, D.J., Bichsel, M. & Wagner, A. 2011. Mobile DNA can drive lineage extinction in prokaryotic populations. J. Evol. Biol. 23: 2422-2431.
42. Sleep, D., Finnis, C., Turner, A. & Evans, L. 2001. Yeast 2 mu m plasmid copy number is elevated by a mutation in the nuclear gene UBC4. Yeast 18: 403-421.
43. Stoebel, D.M., Deant, A.M. & Dykhuizen, D.E. 2008. The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178: 1653-1660.
44. Torres, E.M., Sokolsky, T., Tucker, C.M., Chan, L.Y., Boselli, M., Dunham, M.J. et al. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924.
45. Tsai, I.J., Bensasson, D., Burt, A. & Koufopanou, V. 2008. Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle. Proc. Natl Acad. Sci. USA 105: 4957-4962.
46. Velmurugan, S., Yang, X.M., Chan, C.S.M., Dobson, M. & Jayaram, M. 2000. Partitioning of the 2-mu m circle plasmid of Saccharomyces cerevisiae: functional coordination with chromosome segregation and plasmid-encoded rep protein distribution. J. Cell Biol. 149: 553-566.
47. Velmurugan, S., Mehta, S. & Jayaram, M. 2003. Selfishness in moderation: evolutionary success of the yeast plasmid. Curr. Top. Dev. Biol. 56: 1-24.
48. Watve, M.M., Dahanukar, N. & Watve, M.G. 2010. Sociobiological control of plasmid copy number in bacteria. PLoS ONE 5: Article No.:e9328.
49. Xiao, W. & Rank, G.H. 1996. The 2 mu m plasmid of laboratory yeast strains is a type-1/type-2 hybrid. Yeast 12: 809-813.
50. Xiao, W., Pelcher, L.E. & Rank, G.H. 1991. DNA-sequence divergence and functional conservation at the STB locus of yeast 2μm circle variants. J. Bacteriol. 173: 1181-1186.
51. Xu, Z.J., Mitsui, K., Motizuki, M., Yaguchi, S. & Tsurugi, K. 1999. The DLP1 mutant of the yeast Saccharomyces cerevisiae with an increased copy number of the 2 mu plasmid shows a shortened lifespan. Mech. Ageing Dev. 110: 119-129.