Selection against Heteroplasmy Explains the Evolution of Uniparental Inheritance of Mitochondria

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Mitochondria contain genes that encode the machinery needed to power cells. Unlike the nuclear genome, the mitochondrial genome is typically inherited from one parent only (uniparental inheritance). The most common explanation for uniparental inheritance is the genomic conflict theory, which states that uniparental inheritance evolved to prevent the spread of ‘selfish’ mitochondria that replicate quickly but produce energy inefficiently. Current explanations have a major problem: when using realistic parameters, mathematical models cannot show that uniparental inheritance can replace biparental inheritance. Clearly, we need a new explanation that fits with standard population-genetic theory. Recent evidence suggests cells may incur a cost when they carry multiple types of mitochondria. Here we show mathematically that uniparental inheritance could have evolved to avoid the costs of maintaining multiple mitochondrial lineages within a cell. Our results explain the long-standing evolutionary mystery of uniparental inheritance and provide insight into the evolution of mating types and binary sexes. Selection against heteroplasmy also has implications for the evolution of the mitochondrial genome because new mitochondrial haplotypes always lead to heteroplasmy before becoming fixed in the population. Thus, selection against heteroplasmy may explain why mtDNA coding-genes have slower substitution rates than analogous genes within the nucleus.

Vyšlo v časopise: Selection against Heteroplasmy Explains the Evolution of Uniparental Inheritance of Mitochondria. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005112
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005112

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Zdroje

1. Hadjivasiliou Z, Lane N, Seymour RM, Pomiankowski A. Dynamics of mitochondrial inheritance in the evolution of binary mating types and two sexes. Proc R Soc Lond B Biol Sci. 2013;280(1769):20131920-. doi: 10.1098/rspb.2013.1920 23986113

2. Mishra P, Chan DC. Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol. 2014;15(10):634–46. doi: 10.1038/nrm3877 25237825

3. Grun P. Cytoplasmic genetics and evolution. New York: Columbia University Press; 1976.

4. Cosmides LM, Tooby J. Cytoplasmic inheritance and intragenomic conflict. J Theor Biol. 1981;89(1):83–129. 7278311

5. Hastings IM. Population genetic-aspects of deleterious cytoplasmic genomes and their effect on the evolution of sexual reproduction. Genet Res. 1992;59(3):215–25. 1511870

6. Law R, Hutson V. Intracellular symbionts and the evolution of uniparental cytoplasmic inheritance. Proc R Soc Lond B Biol Sci. 1992;248(1321):69–77. 1355912

7. Bergstrom CT, Pritchard J. Germline bottlenecks and the evolutionary maintenance of mitochondrial genomes. Genetics. 1998;149(4):2135–46. 9691064

8. Hadjivasiliou Z, Pomiankowski A, Seymour RM, Lane N. Selection for mitonuclear co-adaptation could favour the evolution of two sexes. Proc R Soc Lond B Biol Sci. 2012;279(1734):1865–72. doi: 10.1098/rspb.2011.1871 22158961

9. Birky CW. Uniparental inheritance of mitochondrial and chloroplast genes—mechanisms and evolution. Proc Natl Acad Sci USA. 1995;92(25):11331–8. 8524780

10. Birky CW, Strausberg RL, Perlman PS. Vegetative segregation of mitochondria in yeast: estimating parameters using a random model. Mol Gen Genet. 1978;158(3):251–61.

11. Zouros E, Ball AO, Saavedra C, Freeman KR. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA. 1994;91(16):7463–7. 8052604

12. Sharpley MS, Marciniak C, Eckel-Mahan K, McManus M, Crimi M, Waymire K, et al. Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell. 2012;151(2):333–43. doi: 10.1016/j.cell.2012.09.004 23063123

13. Rand DM. The units of selection on mitochondrial DNA. Annu Rev Ecol Syst. 2001;32 : 415–48.

14. Eyre-Walker A, Keightley PD. The distribution of fitness effects of new mutations. Nature Reviews Genetics. 2007;8(8):610–8. 17637733

15. Rossignol R, Faustin B, Rocher C, Malgat M, Mazat JP, Letellier T. Mitochondrial threshold effects. Biochem J. 2003;370(Pt 3):751–62. Epub 2002/12/07. 12467494

16. Hoffmann HP, Avers CJ. Mitochondrion of yeast: Ultrastructural evidence for one giant, branched organelle per cell. Science. 1973;181(4101):749–51. 4579683

17. Beckers MC, Munaut C, Minet A, Matagne RF. The fate of mitochondrial DNAs of mt+ and mt -⁠ origin in gametes and zygotes of Chlamydomonas. Curr Genet. 1991;20(3):239–43. Epub 1991/08/01. 1934130

18. Moriyama Y, Kawano S. Rapid, selective digestion of mitochondrial DNA in accordance with the matA hierarchy of multiallelic mating types in the mitochondrial inheritance of Physarum polycephalum. Genetics. 2003;164(3):963–75. 12871907

19. Silliker ME, Liles JL, Monroe JA. Patterns of mitochondrial inheritance in the myxogastrid Didymium iridis. Mycologia. 2002;94(6):939–46. 21156568

20. Nakamura S. Paternal inheritance of mitochondria in Chlamydomonas. J Plant Res. 2010;123(2):163–70. doi: 10.1007/s10265-009-0295-8 20069335

21. Neale DB, Sederoff RR. Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet. 1989;77(2):212–6. Epub 1989/02/01. doi: 10.1007/BF00266189 24232531

22. Hurst LD, Hamilton WD. Cytoplasmic fusion and the nature of sexes. Proc R Soc Lond B Biol Sci. 1992;247(1320):189–94.

23. Denver DR, Morris K, Lynch M, Vassilieva LL, Thomas WK. High direct estimate of the mutation rate in the mitochondrial genome of Caenorhabditis elegans. Science. 2000;289(5488):2342–4. 11009418

24. Lynch M, Sung W, Morris K, Coffey N, Landry CR, Dopman EB, et al. A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci USA. 2008;105(27):9272–7. doi: 10.1073/pnas.0803466105 18583475

25. Haag-Liautard C, Coffey N, Houle D, Lynch M, Charlesworth B, Keightley PD. Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. PLoS Biol. 2008;6(8):e204. doi: 10.1371/journal.pbio.0060204 18715119

26. Ephrussi B. Nucleocytoplasmic relations in microorganisms. Oxford: Clarendon Press; 1953.

27. Lane N. The problem with mixing mitochondria. Cell. 2012;151(2):246–8. doi: 10.1016/j.cell.2012.09.028 23063117

28. Fan W, Waymire KG, Narula N, Li P, Rocher C, Coskun PE, et al. A Mouse Model of Mitochondrial Disease Reveals Germline Selection Against Severe mtDNA Mutations. Science. 2008;319(5865):958–62. doi: 10.1126/science.1147786 18276892

29. Park JS, Sharma LK, Li H, Xiang R, Holstein D, Wu J, et al. A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Hum Mol Genet. 2009;18(9):1578–89. doi: 10.1093/hmg/ddp069 19208652

30. Picard M, Zhang J, Hancock S, Derbeneva O, Golhar R, Golik P, et al. Progressive increase in mtDNA 3243A>G heteroplasmy causes abrupt transcriptional reprogramming. Proc Natl Acad Sci USA. 2014;111(38):E4033–E42. doi: 10.1073/pnas.1414028111 25192935

31. Wallace DC. Why do we still have a maternally inherited mitochondrial DNA? Insights from evolutionary medicine. Annu Rev Biochem. 2007;76 : 781–821. 17506638

32. Poe BG III, Duffy CF, Greminger MA, Nelson BJ, Arriaga EA. Detection of heteroplasmy in individual mitochondrial particles. Anal Bioanal Chem. 2010;397(8):3397–407. doi: 10.1007/s00216-010-3751-3 20467729

33. Gilkerson RW, Schon EA, Hernandez E, Davidson MM. Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J Cell Biol. 2008;181(7):1117–28. doi: 10.1083/jcb.200712101 18573913

34. Hoekstra RF. Evolution of uniparental inheritance of cytoplasmic DNA. In: Maynard Smith J, Vida G, editors. Organizational constraints on the dynamics of evolution. New York: Manchester University Press; 1990.

35. Lynch M. Mutation accumulation in transfer RNAs: Molecular evidence for Muller's ratchet in mitochondrial genomes. Mol Biol Evol. 1996;13(1):209–20.. 8583893

36. Popadin KY, Nikolaev SI, Junier T, Baranova M, Antonarakis SE. Purifying selection in mammalian mitochondrial protein-coding genes is highly effective and congruent with evolution of nuclear genes. Mol Biol Evol. 2013;30(2):347–55. doi: 10.1093/molbev/mss219 22983951

37. Lynch M. The origins of genome architecture: Sinauer Associates Inc; 2007.

38. Muller HJ. The relation of recombination to mutational advance. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis. 1964;1(1):2–9.

39. Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974;78(2):737–56. 4448362