Selfish drive can trump function when animal mitochondrial genomes compete

Hansong Ma; Patrick H O'Farrell

doi:10.1038/ng.3587

journal article Jun 06, 2016

Selfish drive can trump function when animal mitochondrial genomes compete

Hansong Ma Patrick H O'Farrell

Nature Genetics Vol. 48 No. 7 pp. 798-802 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/ng.3587

Topics

No keywords indexed for this article. Browse by subject →

References

50

[1]

Ma, H., Xu, H. & O'Farrell, P.H. Transmission of mitochondrial mutations and action of purifying selection in Drosophila melanogaster. Nat. Genet. 46, 393–397 (2014). 10.1038/ng.2919

[2]

Hill, J.H., Chen, Z. & Xu, H. Selective propagation of functional mitochondrial DNA during oogenesis restricts the transmission of a deleterious mitochondrial variant. Nat. Genet. 46, 389–392 (2014). 10.1038/ng.2920

[3]

Hurst, G.D. & Werren, J.H. The role of selfish genetic elements in eukaryotic evolution. Nat. Rev. Genet. 2, 597–606 (2001). 10.1038/35084545

[4]

Crow, J.F. Genes that violate Mendel's rules. Sci. Am. 240, 134–143, 146 (1979). 10.1038/scientificamerican0279-134

[5]

Hickey, D.A. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101, 519–531 (1982). 10.1093/genetics/101.3-4.519

[6]

MacAlpine, D.M., Kolesar, J., Okamoto, K., Butow, R.A. & Perlman, P.S. Replication and preferential inheritance of hypersuppressive petite mitochondrial DNA. EMBO J. 20, 1807–1817 (2001). 10.1093/emboj/20.7.1807

[7]

Taylor, D.R., Zeyl, C. & Cooke, E. Conflicting levels of selection in the accumulation of mitochondrial defects in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99, 3690–3694 (2002). 10.1073/pnas.072660299

[8]

Jasmin, J.N. & Zeyl, C. Rapid evolution of cheating mitochondrial genomes in small yeast populations. Evolution 68, 269–275 (2014). 10.1111/evo.12228

[9]

Samuels, D.C. et al. Recurrent tissue-specific mtDNA mutations are common in humans. PLoS Genet. 9, e1003929 (2013). 10.1371/journal.pgen.1003929

[10]

Clark, K.A. et al. Selfish little circles: transmission bias and evolution of large deletion-bearing mitochondrial DNA in Caenorhabditis briggsae nematodes. PLoS One 7, e41433 (2012). 10.1371/journal.pone.0041433

[11]

Phillips, W.S. et al. Selfish mitochondrial DNA proliferates and diversifies in small, but not large, experimental populations of Caenorhabditis briggsae. Genome Biol. Evol. 7, 2023–2037 (2015). 10.1093/gbe/evv116

[12]

Moraes, C.T., Kenyon, L. & Hao, H. Mechanisms of human mitochondrial DNA maintenance: the determining role of primary sequence and length over function. Mol. Biol. Cell 10, 3345–3356 (1999). 10.1091/mbc.10.10.3345

[13]

Volz-Lingenhöhl, A., Solignac, M. & Sperlich, D. Stable heteroplasmy for a large-scale deletion in the coding region of Drosophila subobscura mitochondrial DNA. Proc. Natl. Acad. Sci. USA 89, 11528–11532 (1992). 10.1073/pnas.89.23.11528

[14]

Tsang, W.Y. & Lemire, B.D. Stable heteroplasmy but differential inheritance of a large mitochondrial DNA deletion in nematodes. Biochem. Cell Biol. 80, 645–654 (2002). 10.1139/o02-135

[15]

Celotto, A.M. et al. Mitochondrial encephalomyopathy in Drosophila. J. Neurosci. 26, 810–820 (2006). 10.1523/jneurosci.4162-05.2006

[16]

Celotto, A.M., Chiu, W.K., Van Voorhies, W. & Palladino, M.J. Modes of metabolic compensation during mitochondrial disease using the Drosophila model of ATP6 dysfunction. PLoS One 6, e25823 (2011). 10.1371/journal.pone.0025823

[17]

Ma, H. & O'Farrell, P.H. Selections that isolate recombinant mitochondrial genomes in animals. eLife 4, e07247 (2015). 10.7554/elife.07247

[18]

Stoneking, M. Hypervariable sites in the mtDNA control region are mutational hotspots. Am. J. Hum. Genet. 67, 1029–1032 (2000). 10.1086/303092

[19]

Jamandre, B.W., Durand, J.D. & Tzeng, W.N. High sequence variations in mitochondrial DNA control region among worldwide populations of flathead mullet (Mugil cephalus). Int. J. Zool. 2014, 1–9 (2014). 10.1155/2014/564105

[20]

Wilkinson, G.S., Mayer, F., Kerth, G. & Petri, B. Evolution of repeated sequence arrays in the D-loop region of bat mitochondrial DNA. Genetics 146, 1035–1048 (1997). 10.1093/genetics/146.3.1035

[21]

Lunt, D.H., Whipple, L.E. & Hyman, B.C. Mitochondrial DNA variable number tandem repeats (VNTRs): utility and problems in molecular ecology. Mol. Ecol. 7, 1441–1455 (1998). 10.1046/j.1365-294x.1998.00495.x

[22]

Lewis, D.L., Farr, C.L., Farquhar, A.L. & Kaguni, L.S. Sequence, organization, and evolution of the A+T region of Drosophila melanogaster mitochondrial DNA. Mol. Biol. Evol. 11, 523–538 (1994).

[23]

Chen, S. et al. A cytoplasmic suppressor of a nuclear mutation affecting mitochondrial functions in Drosophila. Genetics 192, 483–493 (2012). 10.1534/genetics.112.143719

[24]

Rand, D.M. Population genetics of the cytoplasm and the units of selection on mitochondrial DNA in Drosophila melanogaster. Genetica 139, 685–697 (2011). 10.1007/s10709-011-9576-y

[25]

Wolff, J.N., Camus, M.F., Clancy, D.J. & Dowling, D.K. Complete mitochondrial genome sequences of thirteen globally sourced strains of fruit fly (Drosophila melanogaster) form a powerful model for mitochondrial research. Mitochondrial DNA http://dx.doi.org/10.3109/19401736.2015.1106496 (2015). 10.3109/19401736.2015.1106496

[26]

Solignac, M., Monnerot, M. & Mounolou, J.C. Concerted evolution of sequence repeats in Drosophila mitochondrial-DNA. J. Mol. Evol. 24, 53–60 (1986). 10.1007/bf02099951

[27]

Tsujino, F. et al. Evolution of the A+T-rich region of mitochondrial DNA in the melanogaster species subgroup of Drosophila. J. Mol. Evol. 55, 573–583 (2002). 10.1007/s00239-002-2353-x

[28]

Schmitz-Linneweber, C. et al. Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase α-subunit mRNA. Plant Cell 17, 1815–1828 (2005). 10.1105/tpc.105.032474

[29]

Meiklejohn, C.D. et al. An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet. 9, e1003238 (2013). 10.1371/journal.pgen.1003238

[30]

Lee, H.Y. et al. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135, 1065–1073 (2008). 10.1016/j.cell.2008.10.047

[31]

Špírek, M., Poláková, S., Jatzová, K. & Sulo, P. Post-zygotic sterility and cytonuclear compatibility limits in S. cerevisiae xenomitochondrial cybrids. Front. Genet. 5, 454 (2014).

[32]

Chen, Z. et al. Genetic mosaic analysis of a deleterious mitochondrial DNA mutation in Drosophila reveals novel aspects of mitochondrial regulation and function. Mol. Biol. Cell 26, 674–684 (2015). 10.1091/mbc.e14-11-1513

[33]

Petit, N. et al. Developmental changes in heteroplasmy level and mitochondrial gene expression in a Drosophila subobscura mitochondrial deletion mutant. Curr. Genet. 33, 330–339 (1998). 10.1007/s002940050344

[34]

Burman, J.L. et al. A Drosophila model of mitochondrial disease caused by a complex I mutation that uncouples proton pumping from electron transfer. Dis. Model. Mech. 7, 1165–1174 (2014). 10.1242/dmm.015321

[35]

Matsuura, E.T., Tanaka, Y.T. & Yamamoto, N. Effects of the nuclear genome on selective transmission of mitochondrial DNA in Drosophila. Genes Genet. Syst. 72, 119–123 (1997). 10.1266/ggs.72.119

[36]

Doi, A., Suzuki, H. & Matsuura, E.T. Genetic analysis of temperature-dependent transmission of mitochondrial DNA in Drosophila. Heredity 82, 555–560 (1999). 10.1038/sj.hdy.6885080

[37]

Dunbar, D.R., Moonie, P.A., Jacobs, H.T. & Holt, I.J. Different cellular backgrounds confer a marked advantage to either mutant or wild-type mitochondrial genomes. Proc. Natl. Acad. Sci. USA 92, 6562–6566 (1995). 10.1073/pnas.92.14.6562

[38]

Niki, Y., Chigusa, S.I. & Matsuura, E.T. Complete replacement of mitochondrial DNA in Drosophila. Nature 341, 551–552 (1989). 10.1038/341551a0

[39]

De Stordeur, E. Nonrandom partition of mitochondria in heteroplasmic Drosophila. Heredity 79, 615–623 (1997). 10.1038/hdy.1997.207

[40]

Saito, S., Tamura, K. & Aotsuka, T. Replication origin of mitochondrial DNA in insects. Genetics 171, 1695–1705 (2005). 10.1534/genetics.105.046243

[41]

van Valen, L. A new evolutionary law. Evol. Theory 1, 1–30 (1973).

[42]

Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation

Mannis van Oven, Manfred Kayser

Human Mutation 2009 10.1002/humu.20921

[43]

McMillan, W.O. & Palumbi, S.R. Rapid rate of control-region evolution in Pacific butterflyfishes (Chaetodontidae). J. Mol. Evol. 45, 473–484 (1997). 10.1007/pl00006252

[44]

Stoneking, M., Hedgecock, D., Higuchi, R.G., Vigilant, L. & Erlich, H.A. Population variation of human mtDNA control region sequences detected by enzymatic amplification and sequence-specific oligonucleotide probes. Am. J. Hum. Genet. 48, 370–382 (1991).

[45]

Townsend, J.P. & Rand, D.M. Mitochondrial genome size variation in New World and Old World populations of Drosophila melanogaster. Heredity 93, 98–103 (2004). 10.1038/sj.hdy.6800484

[46]

Casane, D. & Guéride, M. Evolution of heteroplasmy at a mitochondrial tandem repeat locus in cultured rabbit cells. Curr. Genet. 42, 66–72 (2002). 10.1007/s00294-002-0328-5

[47]

Hoelzel, A.R., Lopez, J.V., Dover, G.A. & O'Brien, S.J. Rapid evolution of a heteroplasmic repetitive sequence in the mitochondrial DNA control region of carnivores. J. Mol. Evol. 39, 191–199 (1994). 10.1007/bf00163807

[48]

Tandemly Repeated Sequences in the Mitochondrial DNA Control Region and Phylogeography of the Pike-PerchesStizostedion

Joseph E. Faber, Carol A. Stepien

Molecular Phylogenetics and Evolution 1998 10.1006/mpev.1998.0530

[49]

Structure and evolution of teleost mitochondrial control regions

Woo-Jai Lee, Janet Conroy, W.Huntting Howell et al.

Journal of Molecular Evolution 1995 10.1007/bf00174041

[50]

Fumagalli, L., Taberlet, P., Favre, L. & Hausser, J. Origin and evolution of homologous repeated sequences in the mitochondrial DNA control region of shrews. Mol. Biol. Evol. 13, 31–46 (1996). 10.1093/oxfordjournals.molbev.a025568

Cited By

75

Evolutionary genetics of the mitochondrial genome: insights from Drosophila

Damian K Dowling, Jonci N Wolff · 2023

Genetics

Mitigation of age-dependent accumulation of defective mitochondrial genomes

Pei-I Tsai, Ekaterina Korotkevich · 2022

Proceedings of the National Academy...

Mitochondrial function in development and disease

Marlies P. Rossmann, Sonia M. Dubois · 2021

Disease Models & Mechanisms

Metrics

75

Citations

50

References

Details

Published: Jun 06, 2016
Vol/Issue: 48(7)
Pages: 798-802
License: View

Authors

Cite This Article

Hansong Ma, Patrick H O'Farrell (2016). Selfish drive can trump function when animal mitochondrial genomes compete. Nature Genetics, 48(7), 798-802. https://doi.org/10.1038/ng.3587

Selfish drive can trump function when animal mitochondrial genomes compete

You May Also Like