The functional transfer of genes from the mitochondria to the nucleus: The effects of selection, mutation, population size and rate of self-fertilization

Genetics

Volumn 182, Issue 4, 2009, Pages 1129-1139

  Brandvain, Yaniv ^a   Wade, Michael J ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; CELL NUCLEUS; FERTILIZATION; GENE LOCUS; GENE MUTATION; GENE NUMBER; GENE TRANSFER; GENETIC SELECTION; HUMAN; MITOCHONDRION; MUTATION RATE; NONHUMAN; POPULATION SIZE; PRIORITY JOURNAL; PROBABILITY;

BIOLOGICAL TRANSPORT; CELL NUCLEUS; EUKARYOTIC CELLS; GENES, MITOCHONDRIAL; INBREEDING; MITOCHONDRIA; MODELS, GENETIC; MUTATION; POPULATION DENSITY; SELECTION, GENETIC;

EUKARYOTA;

EID: 70350176186     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.100024     Document Type: Article

References (59)

1. ADAMS, K. L., and J. D. PALMER, 2003 Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol. Phylogenet. Evol. 29: 380-395.
2. ADAMS, K. L., Y. L. QIU, M. STOUTEMYER and J. D. PALMER, 2002 Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc. Natl. Acad. Sci. USA 99: 9905-9912.
3. AKMAN, L., A. YAMASHITA, H. WATANABE, K. OSHIMA, T. SHIBA et al., 2002 Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32: 402-407.
4. ALBERT, B., B. GODELLE, A. ATLAN, R. DEPAEPE and P. H. GOUYON, 1996 Dynamics of plant mitochondrial genome: model of a three-level selection process. Genetics 144: 369-382.
5. ALLEN, J. F., 1993 Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J. Theor. Biol. 165: 609-631.
6. BERG, O. G., and C. G. KURLAND, 2000 Why mitochondrial genes are most often found in nuclei. Mol. Biol. Evol. 17: 951-961.
7. BLANCHARD, J. L., and M. LYNCH, 2000 Organellar genes - Why do they end up in the nucleus? Trends Genet. 16: 315-320.
8. BOCK, R., and J. N. TIMMIS, 2008 Reconstructing evolution: gene transfer from plastids to the nucleus. BioEssays 30: 556-566. (Pubitemid 351859412)
9. BOORE, J. L., 1999 Animal mitochondrial genomes. Nucleic Acids Res. 27: 1767-1780.
10. BRANDVAIN, Y., M. S. BARKER and M. J. WADE, 2007 Gene coinheritance and gene transfer. Science 315: 1685-1685
11. CHARLES, H., D. MOUCHIROUD, J. LOBRY, I. GONCALVES and Y. RAHBE, 1999 Gene size reduction in the bacterial aphid endosymbiont, Buchnera. Mol. Biol. Evol. 16: 1820-1822.
12. CHO, Y., J. P. MOWER, Y. L. QIU and J. D. PALMER, 2004 Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. Proc. Natl. Acad. Sci. USA 101: 17741-17746.
13. COYNE, J. A., N. H. BARTON and M. TURELLI, 1997 Perspective: a critique of Sewall Wright's shifting balance theory of evolution. Evolution 51: 643-671.
14. COYNE, J. A., N. H. BARTON and M. TURELLI, 2000 Is Wright's shifting balance process important in evolution? Evolution 54: 306-317.
15. DALEY, D. O., and J. WHELAN, 2005 Why genes persist in organelle genomes. Genome Biol. 6: 110-115.
16. FOSTER, J., M. GANATRA, I. KAMAL, J. WARE, K. MAKAROVA et al., 2005 The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3: 599-614.
17. GALLOWAY, L. F., and C. B. FENSTER, 1999 The effect of nuclear and cytoplasmic genes on fitness and local adaptation in an annual legume, Chamaecrista fasciculate. Evolution 53: 1734-1743.
18. GIL, R., B. SABATER-MUNOZ, A. LATORRE, F. J. SILVA and A. MOYA, 2002 Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc. Natl. Acad. Sci. USA 99: 4454-4458.
19. GOODNIGHT, C. J., 1987 On the effect of founder events on epistatic genetic variance. Evolution 41: 80-91.
20. GOODNIGHT, C. J., 1988 Epistasis and the effect of founder events on the additive genetic variance. Evolution 42: 441-454.
21. GOODNIGHT, C. J., and M. J. WADE, 2000 The ongoing synthesis: a reply to Coyne, Barton, and Turelli. Evolution 54: 317-324.
22. GRUN, P., 1976 Cytoplasmic Genetics and Evolution. Columbia University Press, New York.
23. HOSMER, D. W., and S. LEMESHOW, 1989 Applied Logistic Regression. Wiley, New York.
24. KHACHANE, A. N., K. N. TIMMIS and V. DOS SANTOS, 2007 Dynamics of reductive genome evolution in mitochondria and obligate intracellular microbes. Mol. Biol. Evol. 24: 449-456.
25. KLASSON, L., and S. G. E. ANDERSSON, 2004 Evolution of minimal-gene- sets in host-dependent bacteria. Trends Microbiol. 12: 37-43.
26. LANG, B. F., G. BURGER, C. J. OKELLY, R. CEDERGREN, G. B. GOLDING et al., 1997 An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387: 493-497.
27. LOPEZ-FANJUL, C., A. FERNANDEZ and M. A. TORO, 1999 The role of epistasis in the increase in the additive genetic variance after population bottlenecks. Genet. Res. 73: 45-59.
28. LYNCH, M., 2007 The Origins of Genome Architecture. Sinauer Associates, Sunderland, MA.
29. LYNCH, M., B. KOSKELLA and S. SCHAACK, 2006 Mutation pressure and the evolution of organelle genomic architecture. Science 311: 1727-1730.
30. MAROOF, M. A. S., Q. ZHANG, D. B. NEALE and R. W. ALLARD, 1992 Associations between nuclear loci and chloroplast DNA genotype in wild barley. Genetics 131: 225-231.
31. MARTIN, W., B. STOEBE, V. GOREMYKIN, S. HANSMANN, M. HASEGAWA et al., 1998 Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393: 162-165. (Pubitemid 28242254)
32. MARTIN, W., T. RUJAN, E. RICHLY, A. HANSEN, S. CORNELSEN et al., 2002 Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA 99: 1246-1251.
33. MORAN, N. A., 2003 Tracing the evolution of gene loss in obligate bacterial symbionts. Curr. Opin. Microbiol. 6: 512-518.
34. MORAN, N. A., and J. J. WERNEGREEN, 2000 Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15: 321-326.
35. MOWER, J. P., P. TOUZET, J. S. GUMMOW, L. F. DELPH and J. D. PALMER, 2007 Extensive variation in synonymous substitution rates in mitochondrial genes of seed plants. BMC Evol. Biol. 7: 135.
36. MURCHA, M. W., C. RUDHE, D. ELHAFEZ, K. L. ADAMS, D. O. DALEY et al., 2005 Adaptations required for mitochondrial import following mitochondrial to nucleus gene transfer of ribosomal protein S10. Plant Physiol. 138: 2134-2144.
37. PALMER, J. D., K. L. ADAMS, Y. R. CHO, C. L. PARKINSON, Y. L. QIU et al., 2000 Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc. Natl. Acad. Sci. USA 97: 6960-6966.
38. PHILLIPS, P. C., 1996 Waiting for a compensatory mutation: phase zero of the shifting-balance process. Genet. Res. 67: 271-283.
39. POLLAK, P. E., 1991 Cytoplasmic effects on components of fitness in tobacco cybrids. Evolution 45: 785-791.
40. RACE, H. L., R. G. HERRMANN and W. MARTIN, 1999 Why have organelles retained genomes. Trends Genet. 15: 364-370.
41. RAND, D. M., R. A. HANEY and A. J. FRY, 2004 Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19: 645-653.
42. RAND, D. M., A. FRY and L. SHELDAHL, 2006 Nuclear-mitochondrial epistasis and Drosophila aging: introgression of Drosophila simulans mtDNA modifies longevity in D. melanogaster nuclear backgrounds. Genetics 172: 329-341.
43. RISPE, C., and N. A. MORAN, 2000 Accumulation of deleterious mutations in endosymbionts: Muller's ratchet with two levels of selection. Am. Nat. 156: 425-441.
44. SACKTON, T. B., R. A. HANEY and D. M. RAND, 2003 Cytonuclear coadaptation in Drosophila: disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57: 2315-2325.
45. SAMBATTI, J. B. M., D. ORTIZ-BARRIENTOS, E. J. BAACK and L. H. RIESEBERG, 2008 Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecol. Lett. 11: 1082-1091.
46. SELOSSE, M. A., B. R. ALBERT and B. GODELLE, 2001 Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol. Evol. 16: 135-141.
47. SHEPPARD, A. E., M. A. AYLIFFE, L. BLATCH, A. DAY, S. K. DELANEY et al., 2008 Transfer of plastid DNA to the nucleus is elevated during male gametogenesis in tobacco. Plant Physiol. 148: 328-336.
48. TAKAHASI, K. R., and F. TAJIMA, 2005 Evolution of coadaptation in a two-locus epistatic system. Evolution 59: 2324-2332.
49. TAMAS, I., L. KLASSON, B. CANBACK, A. K. NASLUND, A. S. ERIKSSON et al., 2002 50 million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
50. TIMMIS, J. N., M. A. AYLIFFE, C. Y HUANG and W. MARTIN, 2004 Organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5: 123-135.
51. UEDA, M., M. FUJIMOTO, S. ARIMURA, N. TSUTSUMI and K. KADOWAKI, 2008a Presence of latent mitochondrial signal in gene on mitochondrial genome. Mol. Biol. Evol. 25: 1791-1793.
52. UEDA, M., T. NISHIKAWA, M. FUJIMOTO, H. TAKANSHI, S. ARIMURA et al., 2008b Substitution of the gene for chloroplast RPS16 was assisted by generation of a dual targeting signal. Mol. Biol. Evol. 25: 1566-1575.
53. VAN HAM, R., J. KAMERBEEK, C. PALACIOS, C. RAUSELL, F. ABASCAL et al., 2003 Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. USA 100: 581-586.
54. VON HEIJNE, G., 1986 Why mitochondria needs a genome. FEBS Lett. 198: 1-4.
55. WADE, M. J., and C. J. GOODNIGHT, 1991 Wright shifting balance theory - an experimental-study. Science 253: 1015-1018.
56. WADE, M. J., and C. J. GOODNIGHT, 1998 Perspective: the theories of Fisher and Wright in the context of metapopulations: when nature does many small experiments. Evolution 52: 1537-1553.
57. WADE, M. J., and C. J. GOODNIGHT, 2006 Cyto-nuclear epistasis: two-locus random genetic drift in hermaphroditic and dioecious species. Evolution 60: 643-659.
58. WERNEGREEN, J. J., A. B. LAZARUS and P. H. DEGNAN, 2002 Small genome of Candidatus blochmannia, the bacterial endosymbiont of Camponotus, implies irreversible specialization to an intracellular lifestyle. Microbiology 148: 2551-2556.
59. YAMAUCHI, A., 2005 Rate of gene transfer from mitochondria to nucleus: effects of cytoplasmic inheritance system and intensity of intracellular competition. Genetics 171: 1387-1396.