Abstract
We compared the nucleotide substitution pattern over the entire genome of two unique variants of the 6,300-bp selfish DNA (2 μm) plasmid in Saccharomyces cerevisiae. The DNA sequence of the left-unique region is identical among 2-μm variants, while the right-unique region shows substantial divergence. This chimeric pattern cannot be explained by neutral or Darwinian selection models. We propose that horizontal transmission of the 2-μm plasmid coupled with a directed, polarized gene conversion maintains the DNA sequence of the left-unique region, whereas the right-unique region is subject to random drift and Darwinian selection.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Amin AA, Sadowski PD (1988) Synthesis of an enzymatically active FLP recombinase in vitro: search for a DNA-binding domain. Mol Cell Biol 9:1987–1995
Babineau D, Vetter D, Andrew BJ, Gronostajski RM, Protean GA, Beatty LG, Sadowski PD (1985) The FLP protein of the 2 micron plasmid of yeast: purification of the protein from Escherichia coli cells expressing the FLP gene. J Biol Chem 260:12313–12319
Dover G, Flavell RB (1984) Molecular coevolution: DNA divergence and the maintenance of function. Cell 38:622–623
Falco SC, Dumas KS (1985) Genetic analysis of mutants of Saccharomyces cerevisiae resistant to the herbicide sulfometuron methyl. Genetics 109:21–35
Fogel S, Hurst D, Mortimer R (1971) Gene conversion in unselected tetrads from multipoint crosses. Stadler Genet Symp 1:89–110
Futcher AB (1988) The 2μm circle plasmid of Saccharomyces cerevisiae. Yeast 4:27–40
Futcher B, Reid E, Hickey DA (1988) Maintenance of the 2μm circle plasmid of Saccharomyces cerevisiae by sexual transmission: an example of selfish DNA. Genetics 118:411–415
Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580
Hartley JL, Donelson JE (1980) Nucleotide sequence of the yeast plasmid. Nature (London) 286:860–865
Ito H, Jukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cation. J Bacteriol 153:163–168
Jayaram, M (1986) Association of reciprocal exchange with gene conversion between the repeated segments of 2-μm circle. J Mol Biol 191:341–354
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Maruyama K, Hard DJ (1991) Evidence for interspecific transfer of the transposable element murine between Drosophila and Zaprionus. J Mol Evol 33:514–524
McLeod M, Craft S, Broach JR (1986) Identification of the crossover site during FLP-mediated recombination in the Saccharomyces cerevisiae plasmid 2μm circle. Mol Cell Biol 6:3357–3367
Mead DJ, Gardner DCJ, Oliver SG (1986) The yeast 2μm plasmid: strategies for the survival of a selfish DNA. Mol Gen Genet 205:417–421
Milkman R, Stoltzfus A (1988) Molecular evolution of the Escherichia coli chromosome. II. Clonal segments. Genetics 120:359–366
Murray JAH, Cesareni G, Argos P (1988) Unexpected divergence and molecular coevolution in yeast plasmids. J Mol Biol 200:601–607
Nicolais A, Treco D, Schultes NP, Szostak JW (1989) An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae. Nature 338:35–39
Ohta T and Dover GA (1984) The cohesive population genetics of molecular drive. Genetics 108:501–521.
O'Neill SL, Giordano R, Colbert AME, Karr TL, Robertson HM (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89:2699–2702
Rank GH, Xiao W, Kolenovsky A, Arndt G (1988) FLP-FRT mediated intrachromosomal recombination on a tandemly duplicated YEp integrant at the ILV2 locus of chromosome XIII in Saccharomyces cerevisiae. Curr Genet 13:273–281
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, New York
Sharp PM, Li WH (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24:28–39
Sherman F, Fink GR, Hicks JB (1983) Methods in yeast genetics: a laboratory manual. Cold Spring Harbor, New York
Som T, Armstrong KA, Volkert FC, Broach JR (1988) Autoregulation of 2μm circle gene expression provides a model for maintenance of stable plasmid copy levels. Cell 52:27–37
Sun H, Treco D, Szostak JW (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific doublestranded breaks at the ARG4 recombination initiation site. Cell 64:1155–1161
Xiao W, Pelcher LE, Rank GH (1990) Sequence diversity of yeast 2μm RAF gene and its coevolution with STB and REPI. Gene 101:75–80
Xiao W, Pelcher LE, Rank GH (1991a) Evidence for cis- and transacting element coevolution of the 2μm circle genome in Saccharomyces cerevisiae. J Mol Evol 32:145–152
Xiao W, Pelcher LE, Rank GH (1991b) DNA sequence divergence and functional conservation at the STB locus of yeast 2μm circle variants. J Bacteriol 173:1181–1186
Xiao W, Rank GH (1990) Cloning of industrial Saccharomyces-2μm plasmid variants by in vivo site-specific recombination. Plasmid 23:67–70
Xiao W, Rank GH (1993) Polymorphism of 2μm plasmids in industrial strains of Saccharomyces cerevisiae. Appl Microbiol Biotechnol 39:80–86
Author information
Authors and Affiliations
Additional information
Correspondence to: G.H. Rank
Rights and permissions
About this article
Cite this article
Xie, Y., Pelcher, L.E. & Ranks, G.H. Chimeric evolution of the 2-μm genome in Saccharomyces cerevisiae . J Mol Evol 38, 363–368 (1994). https://doi.org/10.1007/BF00163153
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00163153