Rapid evolution of cheating mitochondrial genomes in small yeast populations

Evolution

Volumn 68, Issue 1, 2014, Pages 269-275

  Jasmin, Jean Nicolas ^a,b   Zeyl, Clifford ^a  

^a WAKE FOREST UNIVERSITY   (United States)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

Author keywords

Cost of sex; Experimental evolution; Genetic conflicts; Mitochondrial genetics; Selfish genetic elements; Symbiosis

Indexed keywords

FITNESS; GENOME; MITOCHONDRIAL DNA; OUTCROSSING; PARENTAL CARE; POPULATION BOTTLENECK; REPRODUCTIVE COST; SYMBIOSIS; YEAST;

ARTICLE; CELL RESPIRATION; COST OF SEX; EXPERIMENTAL EVOLUTION; GENETIC CONFLICTS; GENETIC SELECTION; GENETICS; MITOCHONDRIAL GENETICS; MITOCHONDRIAL GENOME; MOLECULAR EVOLUTION; MUTATION; SACCHAROMYCES CEREVISIAE; SELFISH GENETIC ELEMENTS; SYMBIOSIS;

COST OF SEX; EXPERIMENTAL EVOLUTION; GENETIC CONFLICTS; MITOCHONDRIAL GENETICS; SELFISH GENETIC ELEMENTS; SYMBIOSIS;

CELL RESPIRATION; EVOLUTION, MOLECULAR; GENOME, MITOCHONDRIAL; MUTATION; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC;

EID: 84890873513     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12228     Document Type: Article

References (48)

1. Barr, C. M., M. Neiman, and D. R. Taylor 2005. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytol. 168:39-50. doi: 10.1111/j.1469-8137.2005.01492.x.
2. Baruffini, E., T. Lodi, C. Dallabona, and F. Foury 2007. A single nucleotide polymorphism in the DNA polymerase gamma gene of Saccharomyces cerevisiae laboratory strains is responsible for increased mitochondrial DNA mutability. Genetics 177:1227-1231.
3. Bendich, A. J. 1987. Why do chloroplasts and mitochondria contain so many copies of their genome? Bioessays 6:279-282. doi: 10.1002/bies.950060608.
4. Bernardi, G. 2005. Lessons from a small, dispensable genome: the mitochondrial genome of yeast. Gene 354:189-200. doi: 10.1016/j.gene.2005.03.024.
5. Brown, S. W., D. de Sugden, and S. G. Oliver 1984. Ethanol production and tolerance in grande and petite yeasts. J. Chem. Technol. Biotechnol. 34:116-120. doi: 10.1002/jctb.280340208.
6. Burch, C. L., and L. Chao 2000. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406:625-628. doi:10.1038/35020564.
7. Carnevali, F., G. Morpurgo, and G. Tecce 1969. Cytoplasmic DNA from petite colonies of Saccharomyces cerevisiae: a hypothesis on the nature of the mutation 163:1331-1333.
8. Chambers, P., and E. Gingold 1986. A direct study of the relative synthesis of petite and grande mitochondrial DNA in zygotes from crosses involving suppressive petite mutants of Saccharomyces cerevisiae. Curr. Genet. 10:565-571.
9. Chinnery, P. F., D. R. Thorburn, D. C. Samuels, S. L. White, H.-H. M. Dahl, D. M. Turnbull, R. N. Lightowlers, and N. Howell 2000. The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both? Trends Genet. 16:500-505. doi: 10.1016/S0168-9525(00)02120-X.
10. de Visser, J. A. G. M., and D. E. Rozen 2005. Limits to adaptation in asexual populations. J. Evol. Biol. 18:779-788. doi: 10.1111/j.1420-9101.2005.00879.x.
11. Ephrussi, B., and S. Grandchamp 1965. Études de la suppressivité des mutants à déficience respiratoire de la levure I. Existence au niveau cellulaire de divers "degrés de suppressivité". Heredity 20:1-7.
12. Ephrussi, B., H. de Marguerie-Hottinguer, and R. Herschel 1955. Suppressiveness: a new factor in the genetic determinism of the synthesis of respiratory enzymes in yeast. Proc. Natl Acad. Sci. USA 41:1065-1071.
13. Evans, R. J., and G. D. Clark-Walker 1985. Elevated levels of petite formation in strains of Saccharomyces cerevisiae restored to respiratory competence II. Organization of mitochondrial genomes in strains high and moderate frequencies of petite mutant formation. Genetics 111:403-432.
14. Fangman, W. L., J. W. Henly, G. Churchill, and B. J. Brewer 1989. Stable maintenance of a 35-base-pair yeast mitochondrial genome. Mol. Cell. Biol. 9:1917-1921.
15. Frank, S. A. 2003. Repression of competition and the evolution of cooperation. Evolution 57:693-705.
16. Fukuhara, H. 1969. Relative proportions of mitochondrial and nuclear DNA in yeast under various conditions of growth. Eur. J. Biochem. 11:135-139.
17. Gingold, E. B. 1981. Genetic analysis of the products of a cross involving a suppressive "petite" mutant of S. cerevisia. Curr. Genet. 3:213-220. doi: 10.1007/BF00429823.
18. Goldring, E. S., L. I. Grossman, and J. Marmur 1971. Petite mutation in yeast II. Isolation of mutants containing mitochondrial deoxyribonucleic acid of reduced size. J. Bact. 107:377-381.
19. Gore, J., H. Youk, and A. van Oudenaarden 2009. Snowdrift game dynamics and facultative cheating in yeast. Nature 459:253-256. doi:10.1038/nature07921.
20. Grimes, G. W., H. R. Mahler, and P. S. Perlman 1974. Nuclear gene dosage effects on mitochondrial mass and DNA. J. Cell Biol. 61:565-574.
21. Harrison, E., V. Koufopanou, A. Burt, and R. C. Maclean 2012. The cost of copy number in a selfish genetic element: the 2-μM plasmid of Saccharomyces cerevisiae. J. Evol. Biol. 25:2348-2356.
22. Hastings, I. M. 1999. The costs of sex due to deleterious intracellular parasites. J. Evol. Biol. 12:177-183.
23. Hurst, L. D. 1994. Cytoplasmic genetics under inbreeding and outbreeding. Proc. R Soc. B 258:287-298. doi: 10.1098/rspb.1994.0175.
24. MacAlpine, D. M., P. S. Perlman, and R. A. Butow 2000. The numbers of individual mitochondrial DNA molecules and mitochondrial DNA nucleoids in yeast are co-regulated by the general amino acid control pathway. EMBO J. 19:767-775.
25. MacAlpine, D. M., J. Kolesar, K. Okamoto, R. A. Butow, and P. S. Perlman 2001. Replication and preferential inheritance of hypersuppressive petite molecular DNA. EMBO J. 20:1807-1817.
26. McCauley, D. E., and M. S. Olson 2008. Do recent findings in plant mitochondrial molecular and population genetics have implications for the study of gynodioecy and cytonuclear conflict? Evolution 62:1013-1025. doi: 10.1111/j.1558-5646.2008.00363.x.
27. Michaelis, G., S. Douglass, M.-J. Tsai, and R. S. Criddle 1971. Mitochondrial DNA and suppressiveness of petite mutants in Saccharomyces cerevisiae. Biochem. Genet. 5:487-495.
28. Moller, K., L. Olsson, and J. Piskur 2001. Ability of anaerobic growth is not sufficient for development of the petite phenotype in Saccharomyces kluyveri. J. Bact. 183:2485-2489.
29. Murphy, H. A., and C. Zeyl 2012. Prezygotic isolation between Saccharomyces cerevisiae and Saccharomyces paradoxus through differences in mating speed and germination timing. Evolution 66:1196-1209.
30. Nagley, P., and A. W. Linnane 1970. Mitochondrial DNA deficient petite mutants of yeast. Biochem. Biophys. Res. Commun. 39:989-996.
31. Nagley, P., and A. W. Linnane 1972. Biogenesis of mitochondria XXI. Studies on the nature of the mitochondrial genome in yeast: the degenerative effects of ethidium bromide on mitochondrial genetic information in a respiratory competent strain. J. Mol. Biol. 66:181-193.
32. Nunnari, J., W. F. Marshall, A. Straight, A. Murray, J. W. Sedat, and P. Walter 1997. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell. 8:1233-1242.
33. Ogur, M., R. St. John, S. Ogur, and A. M. Mark 1959. The direct estimation of mutation rate from mutant frequency under special conditions. Genetics 44:483-496.
34. Petersen, R. F., R. B. Langkjaer, J. Hvidtfeldt, J. Gartner, W. Palmen, D. W. Ussery, and J. Piskur 2002. Inheritance and organisation of the mitochondrial genome differ between two Saccharomyces yeasts. J. Mol. Biol. 3:627-636. doi: 10.1016/S0022-2836(02)00037-2.
35. Rand, D. M. 2011. Population genetics of the cytoplasm and the units of selection on mitochondrial DNA in Drosophila melanogaster. Genetica 139:685-697.
36. Randerson, J. P., and L. D. Hurst 1999. Small sperm, uniparental inheritance and selfish cytoplasmic elements: a comparison of two models. J. Evol. Biol. 12:1110-1124. doi: 10.1046/j.1420-9101.1999.00112.x.
37. Roze, D., F. Rousset, and Y. Michalakis 2005. Germline bottlenecks, biparental inheritance and selection on mitochondrial variants: a two-level selection model. Genetics 170:1385-1399.
38. Selosse, M.-A., B. Albert, and B. Godelle 2001. Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol. Evol. 16:135-141.
39. Taylor, D. R., C. Zeyl, and E. Cooke 2002. Conflicting levels of selection in the accumulation of mitochondrial defects in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 99:3690-3694.
40. Travisano, M., and G. J. Velicer 2004. Strategies of microbial cheater control. Trends Microbiol. 12:72-78. doi: 10.1016/j.tim.2003.12.009.
41. Tsai, I. J., D. Bensasson, A. Burt, and V. Koufopanou 2008. Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle. Proc. Natl Acad. Sci. USA 105:4957-4962. doi: 10.1073/pnas.0707314105.
42. Uchida, A., and K. Suda 1978. Distribution of mitochondrially inherited drug-resistance genes to tetrads from young zygotes in yeast. Molec. Gen. Genet. 165:191-197.
43. Woods, R. J., J. E. Barrick, T. F. Cooper, U. Shrestha, M. R. Kauth, and R. E. Lenski 2011. Second-order selection for evolvability in a large Escherichia coli population. Science 331:1433-1436. doi: 10.1126/science.1198914.
44. Waxman, W. F., and N. R. Eaton 1974. Nuclear factors and the control of suppressiveness in petite mutants of Saccharomyces cerevisiae. Mol. Gen. Genet. 133:37-45.
45. Waxman, M. F., and C. W. Birky Jr. 1982. Partial pedigree analysis of the segregation of yeast mitochondrial genes during vegetative reproduction. Curr. Gen. 5:171-180.
46. Williamson, D. 2002. The curious history of yeast mitochondrial DNA. Nat. Rev. Gen. 3:475-481. doi:10.1038/nrg814.
47. Zeyl, C., and J. A. G. M. DeVisser 2001. Estimates of the rate and distribution of fitness effects of spontaneous mutation in Saccharomyces cerevisiae. Genetics 157:53-61.
48. Zweifel, S. G., and W. L. Fangman 1991. A nuclear mutation reversing a biased transmission of yeast mitochondrial DNA. Genetics 128:241-249.